Vol. XII

Edited by K.
Kubitzki
Volume XII
Flowering Plants
Eudicots
Santalales, Balanophorales
J. Kuijt, B. Hansen
THE FAMILIES
AND GENERA
OF VASCULAR PLANTS
Edited by K. Kubitzki
For further volumes see list at the end of the book and:
http://www.springer.com/series/1306
.
The Families
and Genera
of Vascular Plants
Edited by K. Kubitzki
XII Flowering Plants Eudicots

Santalales, Balanophorales
Job Kuijt Bertel Hansen
With 82 Figures
Prof. em. Dr. Job Kuijt Dr. Bertel Hansen (deceased)
649 Lost Lake Road formerly at Botanical Museum
Victoria BC V9B 6E3 Copenhagen, Denmark
Canada
Series Editor
Prof. Dr. Klaus Kubitzki

Universit€at Hamburg
Biozentrum Klein-Flottbek und Botanischer Garten
22609 Hamburg
Germany
ISBN 978-3-319-09295-9 ISBN 978-3-319-09296-6 (eBook)

DOI 10.1007/978-3-319-09296-6
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Foreword
Some years ago I sent Prof. Kuijt a photograph of a mistletoe of a genus that is endemic
to southern Chile and Argentina, and largely restricted to the tree genus Nothofagus as
its host. Upon this first contact we found out that we shared great love for the forests of
austral South America, and with some discretion I could familiarize Dr. Kuijt with the
scope and objective of my book series. Throughout his career Dr. Kuijt has made
significant contributions to the morphology, biology and systematics of Santalales,
which in my opinion made him the born author of Santalales for this book series.
Nevertheless, because of the difficulties of the contentious family classification result-
ing from the apparently insurmountable differences between morphological and
molecular data sets, he would have shied from this task had I not helped him to
overcome these difficulties by pointing to the goal of the series, which is not so
much aiming at a definitive family classification but rather trying to provide a broad
factual basis that allows the reader to follow the arguments and form an own concept. I
am particularly thankful to Dr. Kuijt who apart from the taxonomic treatment of
Santalales has also given broad attention to the phenomenon of parasitism with all
its manifestations such as primary haustoria and ramal parasitism, secondary haus-
toria and root parasitism, and the haustorial connection and tissue continuity between
host and parasite, important topics that all have been the subject of Dr. Kuijt’s lifelong
studies. Thus, it remains for me to express to Dr. Kuijt my deepest gratitude for
agreeing to author the present treatment and bringing it to a fortunate end. I am
sure that the present volume will be the pride of my entire series!
The treatment of Balanophoraceae is based on a manuscript prepared about 35
years ago by the late Dr. B. Hansen as one of the first contributions to this book series.
Unfortunately, the author did not live to see publication of his work but his later
publications on the subject allowed me to include further original information both
from his papers and also from other sources. Dr. Hansen will be remembered by the
lasting imprint he left upon this book series, for which his original draft had served as a
kind of starter.
I am also most grateful to the copyright holders who so readily allowed us to
reprint in this volume most valuable illustrations published under their responsibility,
including the Director and Board of Trustees, Royal Botanic Gardens, Kew, the
Secretary of The Flora Malesiana Foundation, Leiden, the New York Botanical Garden
Press, Bronx, New York, and the University of California Press, Berkeley and Los
Angeles.
As usual, the present volume has greatly profited from the critical eyes of the copy
editor Dr. Monique Delafontaine, to whom I am continually grateful for her dedicated
work. Dr. Sabine von Mering deserves my thanks for compiling the index of the
volume. I would also like to gratefully acknowledge the agreeable collaboration with
Dr. Andrea Schlitzberger from the staff of Springer Verlag, and with SPi Technologies
India TvP Limited for type setting and page laying.
Hamburg, 16 August 2014 Klaus Kubitzki

v
.
Acknowledgements
I am indebted to Valéry Malécot for information on Brachynema and Scleropyrum, to

Daniel Nickrent for answers to various literature questions, and to Jim Reveal for
nomenclatural advice. Gerry Allen gave of her time to discuss some technical points on
phylogenetic taxonomy. Paul Hiepko contributed significantly to my understanding of
Opiliaceae. The editor of this series, Klaus Kubitzki, has been extremely helpful during
the preparation of this work. To all, my sincere thanks.
Job Kuijt
vii
.
Contents
SANTALALES
Historical Survey ............................................ 3
Morphology and Anatomy ............................................ 7
Chromosome Numbers and . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Embryology
Fruits, Seeds and Seedlings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Biological and Structural Aspects of . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
Parasitism
Chemosystematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Santalales in Human Affairs and . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
Conservation
Family Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
Key to the Families of Santalales . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
Aptandraceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Coulaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
Eremolepidaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Loranthaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
Misodendraceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121
Octoknemaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
Olacaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Opiliaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
Santalaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
Schoepfiaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
Viscaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
Ximeniaceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
ix
x Contents
BALANOPHORALES
Balanophoraceae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
SANTALALES
By J. Kuijt
Historical Survey
The order Santalales has had a complex history, its (1892) proposed a much wider concept of Lor-
contents and outline undergoing many changes anthaceae that included genera today placed in
over the years, and significant controversies per- Olacaceae, Erythropalaceae, Grubbiaceae, Bala-
sist in our days. A very detailed historical account nophoraceae, and Misodendraceae. While this
was provided by Reed (1955); innumerable genera conception today is of little more than historic
have in the past been placed in the order and interest, we find these families grouped together
subsequently been removed. (For a brief history in the same volume in both editions of Die Nat€ ur-
of neotropical mistletoes, see Kuijt 2014; Table 1.) lichen Pflanzenfamilien. Before the end of the
The affinities between Olacaceae, Lorantha- 19th century, meanwhile, Van Tieghem proposed
ceae and Santalaceae were not beginning to be a profound fragmentation of what we today know
recognized until Brown (1810) first placed the last as Santalales (Van Tieghem 1898), basing at least
two families together. Three years later the “Ola- some of his arguments on the variable structure
cineae” were introduced as a family (Mirbel 1813) of ovules. Since this proliferation of families and
but placed remote from Santalaceae and Lor- orders has not been followed by any subsequent
anthaceae, a suggestion followed by de Candolle worker, it remains as no more than a complex
(1824) who also treated Loranthaceae in a sepa- series of footnotes with little bearing on our pres-
rate volume of his Prodromus (de Candolle 1830). ent insights.
There are cautious hints in Endlicher’s writing A more realistic and modern view of Santa-
(Endlicher 1837) that the three families might be lales was not available until Schellenberg’s pivotal
related, but they remained widely separated in his work (1932). Here we find Olacaceae at the base of
publication. The three families were for the first the various families because of having 0–2 integu-
time united by A. Brongniart (1850), who placed ments, and the Loranthaceae (at that time still
them together in his Class Santalineae, along with including both Viscaceae and Eremolepidaceae)
some doubtful groups. Planchon and Decaisne at the order’s terminus because of the lack of
(1855), agreeing with these suggested affinities, differentiated ovules. Part of Schellenberg’s moti-
added Proteaceae, an affinity that is no longer vation was a perceived gradient of increasing
taken seriously today. It is in that publication parasitism—an idea that, however, inadequately
that we first find the term “calycode” used that, defined or supported, may have been traceable to
in our contemporary terminology, would proba- Van Tieghem’s publications (none of which are
bly compare to “calyculus”. Bentham and Hooker cited in Schellenberg’s work), and was to be
did not follow these French workers; both Lor- repeated by some later students like Reed
anthaceae and Santalaceae are to be found in (1955). However, the resultant more or less linear
volume 3, but “Olacineae” (the present Olacaceae arrangement of families was not always convinc-
and Opiliaceae, but also containing Icacinaceae) ing. Clearly, such ideas have had an influence on
were treated in volume 1 of their Genera Plan- later writers, especially in the second edition of
tarum (Bentham and Hooker 1862–1883). Baillon Die nat€urlichen Pflanzenfamilien.
J. Kuijt and B. Hansen, Flowering Plants. Eudicots, The Families and Genera of Vascular Plants 12, 3
DOI 10.1007/978-3-319-09296-6_1, # Springer International Publishing Switzerland 2015
4 Historical Survey
Table 1 Family disposition of genera of Santalales beyond mistletoes and non-contentious Santalaceae. (For contentious
members of the Santalaceae, see Table 4 under that family.)
Sleumer (1935a, 1935b) or others Nickrent et al. (2010) Present treatment
Anacolosa Olacaceae Aptandraceae Olacaceae
Aptandra Olacaceae Aptandraceae Aptandraceae
Arjona Santalaceae Schoepfiaceae Santalaceae
Brachynema Olacaceae Excluded Olacaceae
Cansjera Opiliaceae Opiliaceae Opiliaceae
Cathedra Olacaceae Aptandraceae Olacaceae
Chaunochiton Olacaceae Aptandraceae Aptandraceae
Coula Olacaceae Coulaceae Coulaceae
Curupira Black and Murça Pires (1948): Olacaceae Ximeniaceae Ximeniaceae
Diogoa Excell and Mendonça (1951): Olacaceae Strombosiaceae ¼ Strombosiopsis
Douradoa Sleumer (1984a, 1984b): Olacaceae Ximeniaceae Ximeniaceae
Dulacia (Liriosma) Olacaceae Olacaceae Olacaceae
Eganthus Olacaceae - ¼ Minquartia
Endusa Olacaceae - ¼ Minquartia
Engomegoma Breteler et al. (1996): Olacaceae Strombosiaceae Olacaceae
Erythropalum Excluded Erythropalaceae Excluded
Harmandia Olacaceae Aptandraceae Aptandraceae
Heisteria Olacaceae Erythropalaceae Olacaceae
Hondurodendron Ulloa et al. (2010): Aptandraceae Aptandraceae Aptandraceae
Liriosma ¼ Dulacia
Maburea Maas et al. (1992): Olacaceae Erythropalaceae Olacaceae
Malania Lee (1980): Olacaceae Ximeniaceae Ximeniaceae
Minquartia Olacaceae Coulaceae Coulaceae
Ochanostachys Olacaceae Coulaceae Coulaceae
Octoknema Octoknemaceae Octoknemaceae Octoknemaceae
Olax Olacaceae Olacaceae Olacaceae
Ongokea Olacaceae Aptandraceae Aptandraceae
Phanerodiscus Cavaco (1954): Olacaceae Aptandraceae Aptandraceae
Ptychopetalum Olacaceae Olacaceae Olacaceae
Quinchamalium Santalaceae Schoepfiaceae Santalaceae
Schoepfia Olacaceae Schoepfiaceae Schoepfiaceae
Scorodocarpus Olacaceae Strombosiaceae Olacaceae
Strombosia Olacaceae Strombosiaceae Olacaceae
Strombosiopsis Olacaceae Strombosiaceae Olacaceae
Tetrastylidium Olacaceae Strombosiaceae Olacaceae
Ximenia Olacaceae Ximeniaceae Ximeniaceae
As mentioned above, the first detailed, port for a relationship of that family with the
general treatment of Santalales is found in the Santalales (Barkman et al. 2007; Su and Hu 2008;
first edition of Die nat€urlichen Pflanzenfamilien. Nickrent et al. 2010). In fact, the occurrence and
In the second edition of this work, more up nature of parasitism in some of the families pres-
to date accounts were provided for Olacaceae ently included has by no means been fully explored
(Sleumer 1935a), Opiliaceae (Sleumer 1935b), beyond the obviously parasitic mistletoes and San-
Octoknemaceae (Mildbraed 1935), Misodendra- talaceae, s.l. Considering the highly advanced
ceae (Skottsberg 1935), Loranthaceae, s.l. (Engler nature of the haustoria in these genera, it is diffi-
and Krause 1935), and Santalaceae (Pilger 1935). cult to conceive of parasitism having evolved in
The order was considered to be allied to some only some genera of a family and not in others.
holoparasitic families (Balanophoraceae, Rafflesia- Undoubtedly, much still needs to be explored in
ceae, Hydnoraceae), but the role of parasitism this regard. A listing of documented parasitism in
appears to have had undue influence in these Santalales is provided in Tables 2 and 3 on p. 2.
assignments. In the case of Balanophoraceae, sur- Families for which the exclusion from Santa-
prisingly, recent molecular data provide some sup- lales is no longer controversial include
References 5
Dipentodontaceae (Worberg et al. 2009), Grub- região Amazônica. Bol. Técn. Inst. Agron. Norte 15:
biaceae (APG II 2003), and Medusandraceae (Sol- 1–32.
Breteler, F.J., Baas, P., Boesewinkel, F.D., Bouman, F.,
tis et al. 2007). More details on the convoluted Lobreau-Callen, D. 1996. Engomegoma Breteler
history of Santalales are found in Harms (1935) (Olacaceae), a new monotypic genus from Gabon.
and Reed (1955). Bot. Jahrb. Syst. 118: 113–132.
Undoubtedly the most significant taxonomic Brongniart, A.T. 1850. Énumération des genres de plantes
cultivés au Muséum d’histoire naturelle de Paris, ed.
development in recent years has been the appli- 2, p. 176.
cation of molecular methods to Santalales, as Brown, R. 1810. Prodromus florae Novae Hollandiae,
seen in the work of D.L. Nickrent and p. 357.
co-workers, especially in Der and Nickrent Brummitt, R.K. 2006. Am I a bony fish? Taxon 55:
268–269.
(2008) and Nickrent et al. (2010). This work has Candolle, A.P. de. 1824. Prodromus systematis naturalis
led to a fundamental revision, at the family regni vegetabilis. 1: 531.
level, of the entire order, and to a new tribal Candolle, A.P. de. 1830. Mémoire sur les Loranthacées.
Coll. Mém. VI: 12.
and subtribal organization of the largest family, Cavaco, A. 1954. Sur le genre Phanerodiscus gen. nov.
Loranthaceae, as presented under that family (Olacacées) de Madagascar. Not. Syst., Paris 15: 10–14.
below. A number of new families were proposed Der, J., Nickrent, D.L. 2008. A molecular phylogeny of
or reinstated from earlier workers, some of Santalaceae (Santalales). Syst. Bot. 33: 107–116.
Endlicher, S.L. 1837. Genera plantarum. Vienna: Fr. Beck.
these proposals appearing to be problematic. Engler, A., Krause, K. 1935. Loranthaceae. In: Engler, A.,
However, this is not an appropriate place to Harms, H., Die nat€ urlichen Pflanzenfamilien, ed. 2,
enter into a detailed consideration of contentious 16b: 98–203.
issues in some of those families, for these will Excell, A.W., Mendonça, F.A. 1951. Novidades de flora de
Angola. Bol. Socied. Broter., ser. 2, 25: 109–110.
be dealt with in the relevant places. The general Harms, H. 1935. Reihen Santalales, Aristolochiales, Bala-
aim of the present treatment is to try and nophorales. In: Engler, A., Harms, H., Die nat€ urli-
reconcile molecular data with morphological chen Pflanzenfamilien, ed. 2, 16b: 1–4.
information wherever resulting in recognizable, Kuijt, J. 2014. Eremolepidaceae, Loranthaceae, and Visca-
ceae. In: Davidse, G. (ed.) Flora Mesoamericana. (in
definable families. I see it as my task to press)
provide a comprehensible account of this highly Lee, S.-K. 1980. Malania, a new genus of oil-yielding
complex order even if occasional apparent con- plant. Bull. Bot. Lab. North-East Forest Inst. 6(8):
flicts with molecular or cladistic indications 67–72.
Maas, P.J.M., Baas, P., Boesewinkel, F.D., Hiepko, P.,
remain (see Nordal and Stedje 2005; Brummitt Lobreau-Callen, D., Van den Oever, L., Ter Welle,
2006; Zander 2011). The main history of conten- B.J.H. 1992. The identity of “Unknown Z”: Maburea
tious genera in the order are indicated in the Maas, a new genus of Olacaceae in Guyana. Bot.
Jahrb. Syst. 114: 275–291.
following table. Mildbraed, J. 1935. Octoknemaceae. In: Engler, A., Harms,
A., Die nat. Pflanzenfam., 2nd edn, 16b: 42–45.
Mirbel, C.F.B. de. 1813. Notes pour servir à l’histoire
References naturelle de la famille des orangers. Nouveau Bull.
des Sciences, par la Société Philomatique 3: 377–382.
Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
APG II (Angiosperm Phylogeny Group). 2003. An update 2010. A revised classification of Santalales. Taxon
of the Angiosperm Phylogeny Group classification 59: 538–558.
for the orders and families of flowering plants: APG Nordal, I., Stedje, B. (coordinators). 2005. Paraphyletic
II. Bot. J. Linn. Soc. 141: 399–436. taxa should be accepted. Taxon 54: 5–6.
Baillon, H.E. 1892. Histoire des plantes 11: 449. Paris: L. Pilger, R. 1935. Santalaceae. In: Engler, A., Prantl, K., Die
Hachette & Cie. nat. Pflanzenfam., 2nd edn, 16b: 52–91.
Barkman, T.L., McNeal, J.R., Lim, S.-H., Croom, H.B., Planchon, J.É., Decaisne, J. 1855. (Communication). Bull.
Young, N.D., de Pamphilis, C.W. 2007. Mitochon- Soc. Bot. France 2: 86–87.
drial DNA suggests at least 11 origins of parasitism Reed, C.F. 1955. The comparative morphology of the
in angiosperms and reveals genomic chimerism in Olacaceae, Opiliaceae and Octoknemaceae. Mem.
parasitic plants. BMC Evol. Biol. 7: 248. Soc. Broteriana 10: 29–79.
Bentham, G., Hooker, J.D. Genera Plantarum, 1862–1883. €
Schellenberg, G. 1932. Uber Systembildung und u €ber die
London: Reeve. Reihe der Santalales. Festschr. Deutsch. Bot. Ges.
Black, G.A., Murça Pires, J. 1948. Dois gêneros novos 50a: 136–145.
Curupira e Froesia, cinco espécies novas, uma nova Skottsberg, C. 1935. Myzodendraceae. In: Engler, A.,
combinação, chaves e observações sobre plantas da Prantl, K., Die nat. Pflanzenfam., 2nd edn, 16b: 92–97.
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Sleumer, H. 1935a. Olacaceae. In: Engler, A., Prantl, K., http://2008.botanyconference.org/engine/search/index.

Die nat. Pflanzenfam., 2nd edn, 16b: 5–32. php?func¼detail&aid¼512.
Sleumer, H. 1935b. Opiliaceae. In: Engler, A., Prantl, K., Ulloa, U.C., Nickrent, D.L., Whitefoord, C., Kelly, D.L.
Die nat. Pflanzenfam., 2nd edn, 16b: 33–41. 2010. Hondurodendron, a new monotypic genus of
Sleumer, H. 1984a. Olacaceae. Flora Malesiana, I, 10: 1–29. Aptandraceae from Honduras. Ann. Missouri Bot.
Sleumer, H. 1984b. Olacaceae. Flora Neotropica 38: 1–159. Gard. 97: 457–467.
New York: Organiz. For Fl. Neotrop. Van Tieghem, P. 1898. Élements de botanique, ed. 3, 2:
Soltis, D.E. et al. 2007. Monophyly and relationships of the 290.
enigmatic amphitropical family Peridiscaceae. Worberg, A. et al. 2009. Huerteales sister to Brassicales
Taxon 56: 65–73. plus Malvales, and newly circumscribed to include
Su, H.-J., Hu, J.-M. 2008. Phylogenetic relationships of Dipentodon, Gerrardina, Huertea, Perrottetia, and
Balanophoraceae and Santalales based on floral B Tapiscia. Taxon 58: 468–478.
homeotic genes. (Abstract 512). Botany 2008. Zander, R.H. 2011. Structuralism in phylogenetic system-
University of British Columbia, Vancouver, B.C. atics. Biol. Theory 5: 383–394.
Morphology and Anatomy
Stem. The stems of members of Santalales are No comprehensive survey of the internal
mostly terete, less commonly ridged or quadran- anatomy of Santalales exists, but Reed (1955)
gular; rarely they are alate or compressed to has provided a detailed summary of Olacacceae,
broadly complanate, as in species of Den- Opiliaceae, and Octoknemaceae. The latter family
drophthora, Exocarpos, Phoradendron, in Phthir- has been updated by Gosline and Malécot (2012),
usa hutchisonii, and especially in many and similar information has been published for
Korthalsella. In Acanthosyris, ramal thorns are some Mexican mistletoes (Gómez-Sánchez et al.
present; this is also said to be true in Ximenia 2011). This information is difficult to summarize
(Sleumer 1935), even though Sleumer’s Fig. 11 for a number of reasons, among which is the
does not show it. inclusion of many generic names in Reed’s work
The great majority of species in Santalales that are not currently accepted, and the use of a
are glabrous or essentially so. Exceptions include complex wood terminology derived from his
Minquartia and Octoknema, which bear elaborate mentor, I.W. Bailey.
stellate epidermal hairs, the short-haired, young Stelar organization has rarely been commen-
portions of Coula, a few species of Phoradendron ted on in the literature, but appears to be of the
and Psittacanthus, especially a number of Lor- standard siphonostelar type. Wilson and Calvin
anthaceae in Africa and Australia, and the genus (1996) have provided information on Arceutho-
Notothixos of Viscaceae that is characterized by bium, where initially a simple siphonostelar
dendritic hairs or peltate scales. arrangement also prevails. However, in at least
Stomatal types are simple and of the rubiac- larger species, the bundles remain separate even
eous type, the guard cells usually being aligned in though they expand tangentially, each curling
slightly oblique positions on stems, as can be seen somewhat laterally. Most species in the genus,
in Oryctanthus grammatus (Kuijt 2011, his being small or even short-lived, are not likely to
Fig. 3a). As in many other plants, abaxial leaf show this pattern. Further information is given in
surfaces tend to have more stomata than adaxial several families below, including the unusual ste-
ones. In Misodendrum subgen. Gymnophyton, the lar structure in Misodendraceae. Other stelar
surface of young stems bears innumerable raised modifications are to be expected in species that
tubercles that each have a stoma at the top, below have evolved phyllodes, as in some species in
which is a large air space. Viscaceae and Exocarpos.
Little or no cork forms in mistletoes, but Nuytsia stems have prominent gum ducts
lenticels are occasionally prominent features, as containing slimy materials.
in Peristethium and stems of Psittacanthus. The With regard to Santalalean wood structure,
trees in the order, of course, have well-developed Reed (1955) has provided many details for Ola-
cork when older, which at times is distinctive in caceae, Opiliaceae, and Octoknemaceae. The
texture or color at the generic level. nodal structure in these families is predominantly
8 Morphology and Anatomy
trilacunar. Anacolosa, Chaunochiton, and Cathe- canthus, Oryctanthus, and in various African
dra have unilacunar nodes, and Scorodocarpus is genera. Linear leaves are found in Amyema gib-
pentalacunar. The arrangement of vessels in the berulum, A. preissii, Lysiana linearifolia and
secondary wood in nearly all genera surveyed is other species in Australia, as well as in some
radial, usually in short series. Heisteria is unusual Thesium and Tripodanthus flagellaris. The fleshy,
in having a diffuse-porous vessel distribution, terete leaves of the xerophytic Psittacanthus
Schoepfia shows a tangential pattern, and some sonorae and Amyema linophylla may be unique
Opiliaceae tend to have solitary vessels. Perfora- in Loranthaceae. Stipules do not exist in the
tion plates are simple except in Engomegoma order. The leaf margin is entire in all but two
(Breteler et al. 1996) and Heisteria (Reed 1955), species: Brachynema ramiflorum has very shal-
where oblique, scalariform perforations occur, as lowly lobed margins, and the leaves of Jodina
they do in Octoknemaceae; lateral walls bear bor- rhombifolia have a prominent marginal spine on
dered pits. Vessels are surrounded by each side.
(sometimes septate) fibers in Octoknemaceae
and Engomegoma, and by tracheids in Heisteria Cataphylls. The term cataphyll, normally describ-
and Opiliaceae, but by libriform fibers ing much reduced phyllomes at the base of a plant
or fiber tracheids in Coulaceae, Chaunochiton, (as in the seedlings of Ximenia, Heckel 1899) or its
Strombosia, Strombosiopsis, Tetrastylidium, ramifications, has specific taxonomic significance
Anacolosa, and Cathedra. Wood parenchyma in several genera of Viscaceae (Kuijt 1959, 1996).
is variously distributed: it is apotracheal in Opi- In Ginalloa and (more irregularly) Notothixos,
liaceae, paratracheal in Schoepfia, and ranges lateral branches bear one pair of inconspicuous,
from diffuse to aggregate in Engomegoma, acute cataphylls that, however, do not provide
Heisteria, Strombosia, Strombosiopsis, Tetrastyli- criteria to distinguish the species. This contrasts
dium, and Coulaceae. Octoknema lacks wood greatly with Dendrophthora and Phoradendron,
parenchyma entirely. In general, many of such where several types of cataphylls occur, supplying
anatomical details are difficult to place in taxo- major systematic criteria. In both genera,
nomic context. numerous species lack cataphylls completely,
Because of the famous oil present in stems especially in the more northern species of
and roots of Santalum album, its wood structure Phoradendron. Perhaps the majority of species,
has received some attention (Metcalfe and Chalk especially in Phoradendron, have one or more
1950). There is little wood parenchyma, and only pairs of basal cataphylls at the lower end of
occasional, scattered vessel members occur, all lateral branches and often also on inflores-
explaining the fine grain of the tree. The xylem cences. In a number of instances, intercalary cat-
consists mostly of fiber tracheids with bordered aphylls and normal foliage leaves alternate on
pits and narrow lumina. The oil of S. album is percurrent stems, in various patterns. Intercalary
present in all cell types. cataphylls in a few cases subtend inflorescences,
Phloem is probably present in all genera but as in the common P. crassifolium.
has received little focused attention in the order.
The curious near-absence of phloem in Arceutho- Prophylls—See under Inflorescences
bium is discussed under Viscaceae.
Secondary phloem tissues containing many Leaf Venation. The great majority of foliar Santa-
clusters of thick-walled sclereids and cells con- lales have pinnately veined leaves, sometimes
taining calcium oxalate crystals and extrastelar very strikingly so, as in Strombosia and Strombo-
fibers are commonly differentiated. siopsis. The common venation pattern is of the
camptodromous type. Palmately veined leaves
Leaf. The leaves of Santalales are uniformly sim- are seen occasionally in Phoradendron—for
ple, but squamate leaves occur in many groups. example, P. chrysocladon—Dendrophthora, Oryc-
The apex is rounded to attenuate, rarely mucro- tanthus, Psittacanthus, Maburea, and elsewhere
nate or emarginate; the base is also variable, in some paleotropical loranthaceous genera. The
mostly being petiolate, occasionally sessile or venation in leafy Misodendrum species is unique
even clasping, as in some Phoradendron, Psitta- in that there are virtually no cross-connections,
Morphology and Anatomy 9
the pattern remaining open (Kuijt 1969). In many and P. pilanthus show a distinctive indumentum,
species of mistletoe, however, the venation is and a few other loranthaceous taxa in the Old
obscure; a striking instance is the Australian World have similarly developed special epider-
Amyema mackayense parasitic on mangroves mal covering. Notothixos may be the only mistle-
that has thick, orbicular leaves storing excess toe genus in which all species are covered with a
salt (Watson 2011, p. 6). dense, gray hair cover. A diagnostic, dense cover
of short, stellate hairs is seen in Octoknema and
Leaf Anatomy. The overall organization of foliar some other Olacaceae, and the staghorn-like mul-
tissues in the order is not unusual, except proba- ticellular hairs of Ximenia are probably unique
bly (but unexplored) in leaves like the terete ones within the order. But all of these are rather excep-
of Psittacanthus sonorae. Sclerenchyma, however, tional. There are numerous genera that are
as far as explored, is extremely variable in Lor- completely glabrous, such as Arceuthobium, Den-
anthaceae, as detailed below. Clusters of storage dropemon, Korthalsella, and Phthirusa in the
tracheids are common throughout Loranthaceae, mistletoes. This does not deny, of course, the
Santalaceae, and Viscaceae, as are crystals of var- instances of internal floral hairs in some groups,
ious sorts; cristarque cells have also been noted in or the setal hairs in Misodendrum. Agonandra
Loranthaceae (Kuijt and Lye 2005). The leaf flower buds have minute glandular structures
mesophyll in Misodendrum is completely undif- that are not, strictly speaking, hairs.
ferentiated (Skottsberg 1935). Laticifers are pres-
ent in the leaves of Chaunochiton, Coula, and Sclerenchyma. Foliar sclerenchyma in Olacaceae
Heisteria (Baas and Kool 1983), and can be recog- and some related families has been detailed by
nized even in dry leaves by holding them up to Baas et al. (1982, and in Maas et al. 1992). Scler-
the light, thus allowing for easy generic identifi- eids are widespread, of brachy- and astroclereids
cation of sterile materials. In Nuytsia, even the as well as columnar types. More infrequent is the
leaf contains conspicuous gum ducts. occurrence of fibrous to filiform astrosclereids.
Maburea has significant bundles of thick-walled
Stomata. Commonly, in the order, stomata are fibers that usually surround the veins (Baas in
more common in the abaxial leaf surface, as in Maas et al. 1992), but lacks sclereids. The diver-
most dicotyledons; however, they may also be sity of occurrence of sclerenchyma types, how-
common on young stems. Only rarely are they ever, does not usually allow convincing
essentially limited to the abaxial leaf surface, as in taxonomic conclusions to be drawn.
Octoknemaceae and Heisteria (Baas and Kool The most detailed presentation of foliar scle-
1983; Gosline and Malécot 2012); frequently, the renchyma in the mistletoes has been that of Kuijt
difference is a matter of degree. In Loranthaceae and Lye (2005), but was limited to neotropical
and Viscaceae, their orientation is mostly Loranthaceae. While much infrageneric variation
(approximately) perpendicular to the length was found, this aspect of leaf anatomy emerged as
direction of the leaf or stem, or slightly oblique. an important source of systematic information in
Detailed information on such aspects, however, is a number of instances. Oryctanthus leaves
lacking. develop a nearly diagnostic type of stellate fiber
bundles that can be recognized even on dry
Indumentum. The great majority of species in leaves. Ligaria shows many isolated, elongated
Santalales have glabrous or essentially glabrous sclereids that are oriented perpendicular to the
leaves. Here and there, in some of the large leaf surface. Aetanthus and Psittacanthus in many
genera, a few species have evolved a recognizable species studied form numerous astrosclereids,
indumentum. For example, two closely related, the length of their arms varying with species,
southern Phoradendron species are densely but some other species lack sclereids completely.
short-tomentose (P. kuntzei, P. tucumanense), Astrosclereids have emerged as a major generic
and some in northwestern Mexico and western character in the newly recognized Peristethium
North America also have a distinctive hair cover, (Kuijt 2012), which includes the species Cladoco-
including especially P. robinsonii and P. veluti- lea roraimensis and Struthanthus leptostachyus as
num. In Psittacanthus, species like P. lasianthus listed in the Kuijt and Lye paper. The most
extraordinary species in this regard is Notanthera Kuijt 1981, his Fig. 17–3), or even from epicortical
heterophylla, the foliar mesophyll of which is roots (Amyema dilatipes, Kuijt 1981, his Fig. 25).
permeated by innumerable, convoluted, slender In certain instances (some Antidaphne; staminate
serpentine fibers that follow erratic paths through Arceuthobium americanum) the concept of inflo-
the leaf. (The astro-filiform sclereids in some rescence is possibly inappropriate. A few cases
species of Heisteria are superficially similar but are seen in Loranthaceae where inflorescences
mostly have a certain amount of branching; Baas do not exist, the flowers being solitary (Kuijt
and Kool 1983.) However, one species, H. cocci- 1981). This is perhaps primitively so in Phthirusa
nea, has unbranched elements remarkably simi- but, in contrast, through reduction in Ligaria and
lar to those of Notanthera. The leaves of Sogerianthe. Finally, the inflorescences of Den-
paleotropical Loranthaceae probably have an drophthora and Phoradendron may have a struc-
equivalent diversity of sclerenchyma, as hinted ture that is unique in flowering plants (Kuijt
by Rao and Kelkar (1951). Amyema pendula 1959), and several instances of flabellate inflores-
from Australia has spectacular, long-armed astro- cences have evolved in the same family.
sclereids as well as clusters of terminal sclereids.
In Viscaceae, leaf sclerenchyma is much more Flowers. As in inflorescence structure, the diver-
simple or rare, but detailed information is not sity of flowers in Santalales is better detailed in
available. Even simpler is the leaf of Misoden- separate families. It is generally agreed that the
drum where no sclerenchyma of any sort is pres- order derives from plants with dichlamydeous
ent, while druses are abundant, as in some perianths and one whorl of stamens. However,
Loranthaceae and Santalaceae. the nature and origin of the perianth continues
to be a controversial subject, and especially pro-
Crystals. The occurrence of crystals in various phylls and the calyx or calyculus require separate
tissues has received less attention than that of discussion.
sclerenchyma, and they are not often of system-
atic use. There seems to be no report of raphides Prophylls. Prophylls (also often called bracteoles
in the order, but all other crystal forms occur in when associated with flowers) have usually been
various groups. Opiliaceae develop no crystals ignored in Santalalean literature, but need to be
(Hiepko 2000), but cystoliths are consistently taken into account in order to comprehend the
present. Cristarque cells, usually in series or clus- morphological architecture of some taxa. In most
ters associated with foliar veins, have been docu- instances they are not recognizable but, paradox-
mented in several Loranthaceous genera (Kuijt ically, branching patterns may indicate a residual
and Lye 2005). The abaxial leaf epidermis of Dio- ability to form secondary lateral branching in
goa, Strombosia, Strombosiopsis, and Tetrastyli- such positions—as it were, in the axils of “phan-
dium contains distinctive, very small cells each of tom” prophylls. This unusual situation is exhib-
which is provided with a central druse. ited clearly in male Arceuthobium americanum,
the normal branching pattern of which is verticil-
Roots—See section on Parasitism late (Kuijt 1970), but also in flower position else-
where in the genus. However, the six branches at
Inflorescences. Inflorescences in Santalales are a node of this species are not equivalent: the two
exceedingly diverse, and do not allow for general- larger ones are axillary to the two scale-leaves at
izations. The relevant comments, therefore, are that node, the four smaller ones in positions
placed in the descriptions of separate families. corresponding to where prophylls might be
Both determinate and indeterminate inflores- expected to exist but are not in evidence. Signifi-
cences may be found in the same family, or even cantly, another Arceuthobium species with the
in the same genus, as in Cladocolea and same branching pattern (A. azoricum) does
Struthanthus. Their position on the plant may indeed show the expected (but unusual) pro-
be axillary or terminal; there are instances phylls (Kuijt 2013). In the genus Psittacanthus,
where inflorescences may emerge endogenously this type of branching may often be seen in vig-
in nodal areas of the stem (see Aetanthus and orous plants while prophylls are scarcely recog-
Psittacanthus), internodes (Dicymanthes seriata, nizable except in a few species—for example,
P. sonorae (Kuijt 2009). In Thesium, the axillary among several other arguments, renders that con-
flowers of many species are flanked by well- cept extremely problematic (Kuijt 2013).
formed prophylls, as is true in Thesidium, but
other species are without (Pilger 1935), while Calyculus. The nature and, indeed, presence of a
most other Santalaceae exhibit no evidence of calyx in Santalales has engendered much debate.
their existence at all. In small-flowered neotropi- The extremes are scarcely in dispute: in Viscaceae
cal Loranthaceae, most genera have well-devel- (notwithstanding the comments of Schaeppi and
oped prophylls accompanying their flowers, Steindl 1945 for female Viscum) and in Misoden-
especially in triadic and dyadic taxa, where the drum there is no evidence of even a reduced calyx
two lateral flowers are placed in the axils of con- (calyculus). In Santalaceae (ignoring the debat-
spicuous prophyllar bracteoles, as in able situation in Buckleya) there is no sign of a
Struthanthus and Passovia, but also in the large- calyculus. In contrast, in some genera of the order
flowered genera Aetanthus and Psittacanthus. In (e.g., Olax and Ongokea), a large calyx completely
Gaiadendron, both bracts and prophylls are foli- envelops the fruit at maturity. The controversy
aceous. Prophylls are small but taxonomically lies in those taxa where there is a more or less
significant in separating Oryctanthus from Mar- discernible rim crowning the ovary, or even
acanthus and certain other genera. In Cladocolea merely a constriction between the ovary and the
and Peristethium, however, monads on inflores- petals. Unfortunately, there are conflicting pub-
cences usually lack visible prophylls. In Olaca- lished reports on some genera, making an accu-
ceae, Strombosiopsis may be the only genus rate summary for the order difficult. As
having each flower subtended by both a bract mentioned above, Nickrent et al. (2010) state
and two prophylls (Sleumer 1935). that Nanodea and Mida have a calyculus, for
In Viscaceae other than Arceuthobium and example, but the primary literature does not
Korthalsella, especially in Dendrophthora and bear this out for the former and is contradictory
Phoradendron, prophylls may be very conspicu- for the latter. Bhatnagar (1960) speaks of a short
ous, and are frequently attested to by the place- and slightly lobed “calyculus” in Mida that is an
ment of secondary branches or inflorescences extremely small, rim-like structure but is not at
(Kuijt 1961, 2003). In the latter two genera, it is all visible in the fruit; yet the detailed illustrations
essential that we distinguish between the frequent of the species (as Fusanus cunninghamii) in
basal cataphylls that are the lowest foliar organs Cheeseman (1914) show nothing of the sort. The
on lateral shoots, and the prophylls that flank morphological nature of the calyculus-like struc-
such branches. The prophylls in these two genera ture in “Strombosiaceae” (Olacaceae) is not clear
are clearly definable. In fact, in certain species of (Nickrent et al. 2010). In Opiliaceae, a calyculus is
Dendrophthora, the two prophylls associated with said to be lacking (Hiepko 1984), but a constric-
a lateral branch may fuse above the branch to tion exists just below the petals with very short
form a double organ, as in D. remotiflora. In D. lobes alternating with the latter. In Aptandraceae
domingensis, all four prophylls of a node may this is true also for the accrescent disk that sur-
fuse into a single compound structure. Finally, rounds the mature drupe in some genera, but in
the multiseriate flower position on inflorescences both Aptandra and Chaunochiton a large, late-
of many Dendrophthora and Phoradendron spe- developing, profusely vasculated funnel would
cies hints at a latent tendency of the node to appear to be a true calyculus (see Kuijt 1969, his
produce flowers in prophyllar positions (Kuijt Figs. 3–20 and 3-23a). In Loranthaceae, the caly-
1961, 2003). culus has been variously interpreted (Kuijt 1969)
From the above it is clear, as also mentioned but is now generally accepted as representing a
elsewhere, that the recent claim (Wanntorp and reduced calyx. In some species it is very incon-
Ronse de Craene 2009) to the effect that the San- spicuous, but in others it may be very large, as in
talalean calyculus represents the developmental Aetanthus mutisii (Kuijt 2014) and especially in
fusion of the prophylls must be rejected. The the recently discovered, second species of Gaia-
separate existence of prophylls and the calyculus dendron (J. Graham and J. Kuijt, in prep.). Signif-
in Oryctanthus and numerous other genera, icantly, the loranthaceous genera usually
regarded as representing basal positions have commonly 4, 5, or 6 (Kuijt 2010). Wanntorp and
vasculated calyculi (Atkinsonia, Garg 1958, Van Ronse de Craene (2009) claimed that, at least in
Tieghem 1895; Desmaria and Gaiadendron punc- Passovia and Struthanthus, the dimorphism of
tatum, Van Tieghem 1895; Nuytsia, Narayana corolla members indicates that the corolla con-
1955). A calyculus is absent only in the male sists of two distinct whorls, but that interpreta-
flower of Tupeia and in some Oryctina. tion is problematic in view of the existence of
The recent claim (Wanntorp and Ronse de Loranthaceae with flowers having odd numbers
Craene 2009) that the calyculus in Santalales of petals or perianths that are sympetalous.
represents a fusion of prophylls must be rejected;
among other reasons, there are a number of Lor- Androecium. The androecium in Santalales is
anthaceous genera in the New World (Mara- exceedingly variable, and the essential details
canthus, Oryctanthus, Oryctina, Struthanthus, will be presented in the separate families. Endress
Panamanthus, Passovia, and Pusillanthus) in (2011) has suggested that, as part of the “core
which prophylls are clearly identifiable in addi- dicots”, there originally may have been two
tion to the calyculus (Kuijt 2013). whorls of stamens, and some surviving evidence
of this might be seen in Heisteria, where one
Perianth. The perianth in Santalales has also been series of stamens opposes the petals and a second
controversial. No problem is encountered in series alternates with them (Sleumer 1935). Rem-
groups in which petals as well as recognizable nants of this pattern also seem to exist in Olax. In
sepals are present. In numerous taxa, however, Coula, however, three stamens oppose each petal
as mentioned earlier, the calyx is exceedingly in addition to those alternating with them. Lir-
small or even questionable and, in many publica- iosma (Dulacia) flowers show fertile anthers
tions, it has been felt that the term tepal is neces- alternating with petals while curious, forked, ster-
sary for the floral organs associated with the ile ones oppose the petals, structures also found
stamens where a calyx is not, or not clearly, rec- in some Olax. The suggested double ancestral
ognizable. A transitional situation is seen where stamen series, therefore, is by no means estab-
the calyx (or calyculus) is extremely small at lished for the order. In the great majority of
anthesis but develops strongly during fruit matu- bisexual or male flowers in Santalales we find
ration, as is seen in certain Aptandraceae and each petal associated with a single stamen, the
others. Past debates on the nature of the petals two elements often basally connate.
in the Santalales have invariably focused on the There are various degrees of filament reduc-
presence or absence of a calyx or calyculus. I am tion even though filaments may also be exceed-
suggesting that a focus on the stamens gives us a ingly long and slender, as in many large-flowered
more informative and conclusive view. Through- Loranthaceae as well as in Chaunochiton. The
out the order—allowing for some irregularities in ultimate reduction finds the anther directly con-
a few Olacaceae—stamens are opposite (and fre- nate with the supporting petal, as in several Vis-
quently basally connate with) the organs in ques- cacean genera, Peristethium, and a scattering of
tion. This is true even where, as in Opiliaceae and other species. Such fusion in Viscum album has
Loranthaceae, a calyculus (a presumed reduced resulted in nothing more than a cushion with
calyx) is definable. I suggest, therefore, that the sporogenous cell clusters.
presence and position of stamens may identify Synandria have evolved in three separate
the true petals. Since the floral organs associated taxa. In some African Viscum, anthers are united
with the stamens clearly are homologous in a central cone (Kuijt et al. 1979), dehiscing
throughout the order, I maintain the term petal extrorsely. In Korthalsella, a central fusion has
for them in the present account. also evolved, this compound structure being
The number of perianth members in Santa- introrsely dehiscent and having a common distal
lales (ignoring the absence of them in male Mis- pore through which pollen grains are liberated
odendraceae and some Antidaphne) ranges from (Mekel 1935). A very different type of synan-
2 or 3 in Arceuthobium to 7 in Gaiadendron drium is present in Aptandra, Harmandia, and
punctatum and 6–8 in Nuytsia, but is more Ongokea, where at least the filaments are connate
into a tube surmounted by a ring of anthers, the (e.g., Coulaceae). The idea is traceable back to at
tip of the stigma being exposed distally (Kuijt least Schellenberg’s work (1932), and is conceiv-
1969, his Figs. 3–19 b and d). ably based on Van Tieghem’s writing. The sepa-
In addition to stamens, Opiliaceae and rate evolution of an ovarian papilla in the various
Aptandra develop fleshy, non-vasculated struc- taxa mentioned above also renders a necessary
tures at the base of the filaments that have defied connection unlikely. In any case, a logical con-
morphological interpretation. In the latter genus, nection is difficult to establish. It may be sug-
a fleshy rim in that position eventually grows out gested that elaborate tissue modifications in
to what may be an aril below the fruit. fruits that relate to dissemination and establish-
In several Loranthaceous genera—for exam- ment of mistletoes require antecedent meriste-
ple, in some Aetanthus and Psittacanthus spe- matic conditions of the ovary, but this is not a
cies—the elongated anthers are subdivided into convincing argument for the great majority of
small clusters of sporogenous tissue, some of Santalalean species that are of a terrestrial germi-
which appear to dehisce separately, rendering nation pattern.
the anther alveolar. The most extraordinary A great deal of morphological reduction has
stamens in the order are found in some African indeed occurred in the evolution of some Santa-
genera of Loranthaceae in which a tension devel- lalean groups, and some of this has concerned a
ops in the bud that allows the entire anther to be number of students who aimed at a precise ter-
shot off suddenly when the flower is opened by a minology. Leaf reduction is common in many
pollinating bird (Kirkup 1998). taxa, exclusively so in genera like Arceuthobium
Mention should also be made of epidermal and Korthalsella. There is a strong trend in ovary
hairs that are closely associated with the stamens reduction, especially in the frequently ategmic
in some taxa. Tufts of hairs are characteristically ovules. In extreme cases, the ovarian cavity has
developed near the stamen insertion in Santala- a central, basal “ovarian papilla” or “mamelon”
ceae. In numerous Psittacanthus species (Kuijt in which embryo sacs differentiate, as in mistle-
2009), there are very prominent, long, shiny toes (including Phacellaria), Agonandra, Antho-
hairs that occupy a similar position, or may be bolus, Exocarpos, and Quinchamalium. In some
attached to the back of anthers or even to the species, even such a structure has disappeared
filaments. Cladocolea biflora, finally, is unique completely, and the embryo sacs are initiated in
in its poststaminal cluster of stiff bristles. The the solid base of the ovary. Furthermore, even the
function of such hairs has not been elucidated ovarian cavity itself may have disappeared, as in
but, in Santalaceae and others, they may be of Viscum and Passovia pyrifolia. The absence of
significance in secondary pollen presentation. integuments has led some students to maintain
that seeds do not, strictly speaking, exist, but that
Gynoecium. The number of carpels originally appears not to be a useful view, as the
involved in the ovary of Santalales has been com- corresponding structure includes an embryo
mented on a few times but generally has been and (with a couple of exceptions) a certain
wisely avoided as a topic because of the high amount of endosperm, the combination being
degree of evolutionary reduction. The number surrounded by a protective layer.
of ovarian cavities or lobes, of ovules and of Perhaps more appealing is the suggestion that
stigmatic lobes gives no guidance in this respect, the extraordinary, aggressive behavior of the
as is demonstrated in Myoschilos, where 3–5 embryo sac of many members of the order
ovules and 2–5 stigmatic lobes are reported per is somehow related to the fact of parasitism.
flower. Vasculation, similarly, offers no convinc- There are numerous instances where part of
ing information. the female gametophyte, or even of the
Since there have been implications in the endosperm, grows aggressively into the tissues
literature to the effect that at least ovular reduc- nearby, whether they be the ovarian papilla,
tion is in some way related to the parasitic mode the ovarian wall, the receptacle, or the style.
of life (Sleumer 1935; Reed 1955; Cronquist 1981), The suggested correlation does, indeed, seem
it is useful to point out that there are non-para- to have some support in that the Santalalean
sitic taxa where ovular reduction is also visible genera in which such phenomena take place are
all parasitic. The one (apparently) non-parasitic cal Loranthaceae, appears to be a convincing
genus in the order that has been studied embryo- documentation of such mistletoes in Middle
logically (Strombosia), as far as I am aware, Eocene North America (Taylor 1989), with simila-
retains its mature embryo sac within the rities to present-day Tripodanthus acutifolius.
ovule (Agarwal 1961). However, numerous non- An intriguing case is in the undoubted fossil
parasitic genera have not yet been studied in loranthaceous pollen from Tasmania, since no
this regard, and it is premature to confirm the mistletoes are known from the island at present.
suggested correlation. The pollen dates from about 100,000 BP, the
A curious historical misinterpretation was island having separated from Australia about
initiated by Gagnepain and Boureau (1947) and 15,000 BP (Watson 2011).
was based on the reduced construction of the
santalaceous ovule. They erected a new genus
and species, Sarcopus aberrans Gagn., being con-
References
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Bonneville, R., Lobreau, D., Riollet, G. 1982. Pollen fossile
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fore discussed under the separate families where d’Oldouvai en Tanzanie: implications paléoécologi-
information is available. Most common is the ques. J. Biogeogr. 9: 469–486.
triporate or tricolporate condition and Breteler, F.J., Baas, P., Boesewinkel, F.D., Bouman, F.,
Lobreau-Callen, D. 1996. Engomegoma Breteler (Ola-
limited sculpturing. Unique pollen types are caceae), a new monotypic genus from Gabon. Bot.
known in unexpected systematic positions, as in Jahrb. Syst. 118: 113–132.
Aptandra zenkeri (Aptandraceae; Bonneville et al. Cheeseman, T.F. 1914. Illustrations of the New Zealand
1982), Arjona (Santalaceae; Lobreau-Callen 1982) flora, 2: 1–2, Pl. 177.
Cronquist, A. 1981. An integrated system of classification
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(Feuer and Kuijt 1980), Oryctanthus, and Phthir- Endress, P. 2011. Evolutionary diversification of the flow-
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Feuer, S., Kuijt, J. 1979. Fine structure of mistletoe pollen.
When we come to reports on fossil Santalalean II. Pollen morphology and evolution in the genus
pollen, we are faced with serious problems of Psittacanthus Mart. Bot. Not. 132: 295–309.
assignment. A striking example is the report of Feuer, S., Kuijt, J. 1980. Fine structure of mistletoe pollen.
Aetanthus pollen from the Oligocene of Puerto III. Large-flowered neotropical Loranthaceae and
their Australian relatives. Amer. J. Bot. 67: 34–50.
Rico (Graham and Jarzen 1969). Aetanthus at pres- Feuer, S., Kuijt, J. 1985. Fine structure of mistletoe pollen.
ent is a small genus restricted to higher Andean VI. Small-flowered neotropical Loranthaceae. Ann.
elevations (Kuijt 2014); it is closely related to the Missouri Bot. Gard. 72: 187–212.
much larger, low-elevation genus Psittacanthus in Gagnepain, F., Boureau, E. 1947. Une nouvelle famille de
Gymnospermes: les Sarcopodacées. Bull. Soc. Bot.
which we find a great diversity of pollen types France 93: 313–320.
(Feuer and Kuijt 1979). The report of Aetanthus Garg, S. 1958. Embryology of Atkinsonia ligustrina (A.
is thus not reliable. In the same way, older reports Cunn. ex F. Muell.) F. Muell. Nature (London) 182:
of fossil pollen in the order, predating more recent 1615–1616.
Gómez-Sánchez, M., Sánchez-Fuentes, L.J., Salazar-Olivo,
work, cannot always be taken seriously. Ximenia L.A. 2011. Anatomı́a de especies mexicanas de los
pollen from the Lower Pleistocene of Olduvai, géneros Phoradendron y Psittacanthus, endémicos
Tanzania, has been recorded (Bonneville et al. del Nuevo Mundo. Revista Mex. de Biodiversidad
1982); the illustrations are similar to extant pollen 82: 1203–1208.
Gosline, G., Malécot, V. 2012. A monograph of Octoknema
of Loranthaceae. A Tennessee report of Gothani- (Octoknemaceae-Olacaceae s.l.). Kew Bull. 66:
pollis, a form genus linked to the extant neotropi- 367–404.
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11: 401–408. Korthalsella dacrydii. Blumea 1: 312–319.
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Australia, 22: 26–29. dons. Oxford: Clarendon Press.
Hiepko, P. 2000. Opiliaceae. Flora Neotropica 82: 1–53. Narayana, R. 1955. Floral morphology and embryology of
Kirkup, D. 1998. Pollination mechanisms in African Lor- Nuytsia floribunda (Labill.) R. Br. Proc. 42nd Indian
anthaceae. In: Polhill, R., Wiens, D., Mistletoes of Sci. Congress, pp. 239–240.
Africa, pp. 37–60. Kew: Royal Bot. Gardens. Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
Kuijt, J. 1959. A study of heterophylly and inflorescence 2010. A revised classification of Santalales. Taxon
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Chromosome Numbers and Embryology
Chromosome Numbers. A listing of known chro- The embryology of Loranthaceae forms a

mosome numbers for the order is found in an suitable introduction. The first satisfactory
electronic supplement attached to Nickrent et al. account is found in the writing of Melchior
(2010). They are reported under individual Treub (1881), director of the Buitenzorg (Bogor)
families where known. Botanical Gardens for nearly three decades
(1880–1909). Numerous subsequent papers dealing
Embryology. The information available on the with Loranthaceae were summarized by Mahesh-
events occurring in and around the embryo sac wari et al. (1957), Kuijt (1969), and Bhandari and
in Santalales is both extraordinary and taxonom- Vohra (1983).
ically uneven. In Loranthaceae, nearly all pub- No individual ovules can be discerned in Lor-
lished work is based on paleotropical genera, anthaceae. Instead, there exists an ovarian papilla
neotropical ones remaining essentially unex- or mamelon placed basally in the unilocular
plored. The few Viscacean genera that have been ovary. The papilla extends far into the style in
studied are, from this point of view, among the Lepeostegeres, and somewhat less so in Nuytsia.
less exotic ones (Bhandari and Vohra 1983; Zaki In Lysiana, instead, there is a central column; in
and Kuijt 1994, 1995); the same may be said about Taxillus, neither papilla nor central column
Misodendraceae (Skottsberg 1935). In the current exists, the archesporial tissue originating directly
families that at one time belonged to Olacaceae, below the narrow ovarian cavity. Completely
and in Opiliaceae, the record is very uneven. solid ovaries are reported for Tupeia (Smart
Nevertheless, the genera studied have yielded 1952), Passovia (Kuijt and Weberling 1972), and
exceptionally interesting data, showing numer- Viscum (Schaeppi and Steindl 1945; Zaki and
ous features that are unique in flowering plants. Kuijt 1994, 1995). Where papillas are present,
The very incomplete record makes it impossible the sporogenous cells may originate in their low-
to draw systematic conclusions on this basis even est lobes; in Lysiana, they are formed in the flanks
within Loranthaceae where most of the work has of its central column. The number of embryo sacs
been done; it is therefore not surprising that per flower varies; it may be that in Passovia pyr-
embryology is scarcely referred to in the modern ifolia and Struthanthus vulgaris only a single
studies of Malécot et al. (2004), Malécot and embryo sac is formed (Venturelli 1981), but in
Nickrent (2008), and Nickrent et al. (2010). Nuytsia there are said to be 6–17 per flower (Nar-
Most of the original, relevant publications date ayana 1955).
from the years of the Maheshwari-Johri school of Whatever the origin of the embryo sacs, they
embryology (1950s and 1960s). Because of the grow upwards into the style, each carrying its egg
many taxonomic changes that have taken place cell and synergids at the apex. The height to
in the order, it seems more appropriate to present which the egg apparatus ascends appears to differ
a general survey of these aspects here. between genera; in one of the most extreme cases
18 Chromosome Numbers and Embryology
(Helixanthera ligustrina), it eventually finds itself

at the stigmatic surface and pushes epidermal
cells out of the way, exposing the tip of the
embryo sac (Fig. 1). In Moquiniella rubra, the
embryo sac reaches the stigmatic surface but
then turns around and grows down a little (Johri
and Raj 1965). Eventually the pollen tube reaches
the egg, and fertilization occurs in situ. A system
of suspensor cells is now formed that pushes the
several proembryos back into the ovary, the fur-
thest one developing into the solitary embryo. All
other proembryos are suppressed and reab-
sorbed. The fate of the early endosperm is poorly
documented: it is not known where the primary
endosperm cell is fertilized, or whether suspensor
cells are formed to facilitate its downward move-
ment. At any rate, the eventual endosperm is
derived from more than one embryo sac, for
example in Nuytsia (Narayana 1955), but also in
other genera. In three genera of the order
(Aetanthus, Psittacanthus, and Lepidoceras), the
endosperm either fails to develop, or is reab-
sorbed during fruit differentiation. In Psitta-
canthus, an extremely massive suspensor body
develops that is later crushed (Kuijt 1967).
The extraordinary events summarized above
have never been given a functional explanation.
The active competition between the embryo
sacs and, later, between the proembryos of a
flower seems to provide an addition to the usual
competition between pollen tubes, thus providing
a triple competitive system in generating the
eventual embryo.
Ovarian structure of Santalaceae also features
a single ovarian chamber, even though (as in
some Loranthaceae) this may be basally lobed.
As mentioned earlier, in several genera (Antho-
bolus, Exocarpos, Phacellaria, Quinchamalium)
there exists a simple ovarian papilla as in most
Loranthaceae, but the more common situation
involves a frequently convoluted, erect funiculus
with three apically suspended, reduced ovules.
Fig. 1. A Helixanthera ligustrina, longitudinal section of
One embryo sac develops in each ovule and gynoecium with mature embryo sacs (x 14). B Detail of
(in Comandra) sends out a lateral caecum just embryo sac on far right in A (x 420). C Tolypanthus
below the egg apparatus that grows out into lagenifer, two-celled proembryo (x 450). D Same, biseriate
the twisted funiculus for some distance. After proembryo (x 450). E Nuytsia floribunda, upper end of
embryo sac with lateral caecum. (Kuijt 1969, redrawn
double fertilization takes place in the upper from Maheswari et al. 1957)
part of the embryo sac, endosperm haustoria are
formed that follow the path of the caecum into the all ovular tissues as well as some adjoining ovary
funiculus. Only a single seed is formed per tissues are suppressed and reabsorbed. In one
flower, and in the course of its early development instance (Santalum: Paliwal 1956), it is reported
Chromosome Numbers and Embryology 19
that—as in most Loranthaceae—the resultant fragmentary information be thought to be repre-

endosperm is also derived from several endo- sentative of individual families.
sperm nuclei. The ovule in these groups shows varying
The embryology of Quinchamalium provides degrees of reduction; the distinction between
additional complications (Johri and Agarwal nucellus and integuments is frequently not
1966). The embryo sac pole housing the egg sharp. In Coula and Minquartia, two integuments
apparatus enlarges in a clavate fashion. The two are recognizable as well as a thin-layered nucel-
synergids, well before fertilization, each form a lus, and the embryo sac remains more or less
tube-like process that traverses the cavity space isodiammetric. In contrast, in Olax and Ptycho-
and grows into the style for about 1/3 of its petalum, no differentiation into nucellus or inte-
length, following its vascular strands. Meanwhile, guments occurs. Here the embryo sac is said to
the antipodal end of the embryo sac is sealed become a convoluted tube breaking out of the
off by a cross wall. The resultant distal portion ovule and into the base of the stylar canal (Fager-
of the embryo sac also elongates and produces a lind 1947), but Agarwal (1963) writes that it
branching system into the ovarian papilla. After remains in the ovule in Olax. Tetrastylidium is
fertilization has occurred, even endosperm cells an example of unitegmic ovules. Aptandra and
form tubular extensions into the apex of the Chaunochiton have embryo sacs that become
papilla. Extraordinarily, the embryo sac of curved, conical structures scarcely emerging
Quinchamalium thus involves three separate from the ovarian papilla, but in Schoepfia the
sets of cellular haustorial structures. embryo sac grows into the ovarian space. Xime-
Equally unusual is the embryology of Exocar- nia has four elongated, pendent ovules. The
pos (Fagerlind 1959; Ram 1959). Here, the embryo above indications are derived from Fagerlind’s
sac absorbs most of the ovarian papilla, forming a work (1947), parts of which require more detailed
number of digital processes downwards. The cav- confirmation.
ity eventually is filled with a polyp-like embryo In Opiliaceae, Cansjera and Opilia have been
sac that also provides upward extensions, some- studied embryologically. In Opilia amentacea, the
times far into the style. It is clear that many chalazal cell of the embryo sac becomes a straight,
further, unusual situations may be expected in tubular, unbranched structure that grows
the numerous Santalaceae that remain unstudied. towards (and even into) the floral base, fertiliza-
Misodendraceae. The pistillate flower of Mis- tion taking place in the top of the embryo sac
odendrum is about 5 mm long, and has a simple (Swamy and Rao 1963). This long, tubular cell
ovarian chamber. As in most Santalaceae, a funic- remains uninucleate, and may be considered
ulus rises from the base, and bears three reduced haustorial in function. Cansjera shows similar
ovules pendent from its apex. Within each ovule, phenomena, but there the haustorial cells branch
one embryo sac develops, the slender antipodal profusely at the tip, and nearby endosperm cells
pole elongating into a tube that grows into the top produce parallel, branched haustoria (Swamy
of the funiculus. The other pole of the embryo sac 1960).
becomes clavate and contains the egg apparatus. The standard typology of embryo sacs has in
It is in that location that the embryo develops. the past been used to characterize some families
From the early endosperm cells, a slender, haus- in Santalales. Loranthaceae and Viscaceae, espe-
torium-like, uninucleate tube forms that retraces cially, have been so designated. The Polygonum
the path of the antipodal haustorium, following type of embryo sac has been used to characterize
the vascular strand down to the base of the funic- Loranthacaee as well as most other members of
ulus, where its tip ramifies somewhat near major the order except Viscaceae, Buckleya (Raj 1964),
vascular strands (Skottsberg 1913). The endo- and Olax, the last three groups having an Allium
sperm of Misodendraceae, as in Viscaceae and a type embryo sac (in Olax, both Allium and Polyg-
few Loranthaceae, is chlorophyllaceous. onum types occur; Agarwal 1963). Once again,
Turning now to the remainder of Santalalean however, the gaps in the record prevent us from
families, all we can do is to report on individual evaluating the taxonomic value of such distinc-
genera without being directly concerned about tions. It is especially noteworthy that Zaki and
their familial positions; in no sense can this Kuijt (1995) came to the conclusion that in one
20 Chromosome Numbers and Embryology
species, Viscum minimum, both of the above Kuijt, J., Weberling, F. 1972 (1973). The flower of Phthir-
types occur, as in Olax. usa pyrifolia (Loranthaceae). Ber. Deutsch. Bot. Ges.
85: 467–480.
In the entire order Santalales, it can thus be Maheshwari, P., Johri, B.M., Dixit, S.N. 1957. The floral
seen that an unbroken gradient of reduction is morphology and embryology of the Loranthoideae
present in the structure of ovules. A standard (Loranthaceae). J. Madras Univ. B, 27: 121–136.
construction, including two integuments and a Malécot, V., Nickrent, D.L. 2008. Molecular phylogenetic
relationships of Olacaceaea and related families.
nucellus, forms one end of this spectrum. There Amer. J. Bot. 33: 97–106.
are also taxa with only one integument, and those Malécot, V., Nickrent, D.L., Baas, P., Van den
where no visible distinction between nucellus and Oever, L., Lobreau-Callen, D. 2004. A morphological
integuments remains. In a number of advanced cladistic analysis of Olacaceae. Syst. Bot. 29: 569–586.
Narayana, R. 1955. Floral morphology and embryology of
taxa, independently in several families, even the Nuytsia floribunda (Labill.) R. Br. Proc. 42nd Indian
ovule is no longer recognizable and is replaced Sci. Congress, pp. 239–240.
with a basal ovarian papilla containing archespor- Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
2010. A revised classification of Santalales. Taxon
ial tissue. This is especially characteristic of the 59: 538–558.
largest mistletoe family, Loranthaceae, but is not Paliwal, R.L. 1956. Morphological and embryological
limited to it. Even greater reduction is seen in some studies in some Santalaceae. Agra Univ. J. Res. 5:
mistletoes where the ovarian papillas also has dis- 193–284.
Raj, B. (1963) 1964. Female gametophyte of Buckleya
appeared, embryo sacs originating in the tissue lanceolata Sieb. et Zucc. (Abstr.). Proc. 50th Indian
below the ovarian cavity. The endpoint of the Sci. Congress (Delhi) 3: 389–390.
reductional gradient is present where even the Ram, M. 1959. Morphological and embryological studies
ovarian cavity no longer exists, the archesporial in the family Santalaceae – II. Exocarpus, with a
discussion on its systematic position. Phytomor-
tissue being initiated in the middle of a solid ovary. phology 9: 4–19.
Schaeppi, H., Steindl, F. 1945. Bl€ utenmorphologische
und embryologische Untersuchungen an einigen
Viscoideen. Vierteljahrsschr. Naturforsch. Gesellsch.
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Skottsberg, C. 1913. Morphologische und embryologische
Agarwal, S. 1963. Morphological and embryological stud- Studien u €ber die Myzodendraceen. Kungl. Sv.
ies in the family Olacaceae I. Olax L. Phytomorphol- Vetensk. Akad. Handl. 51(4): 1–34, Tab. 1.
ogy 13: 185–196. Skottsberg, C. 1935. Myzodendraceae. in A. Engler and
Bhandari, N.N., Vohra, S.C.A. 1983. Embryology and affi- K. Prantl, eds. Die Nat€ urlichen Planzenfamilien
nities of Viscaceae. In: Calder, M., Bernhardt, P. (K. Die. Nat. Pfl. Fam.), ed. 2, 166: 92–97
(eds.) The biology of mistletoes, pp. 69–86. Sydney: Smart, C. 1952. The life-history of Tupeia Cham. et Schl.
Academic Press. Trans. Roy. Soc. N. Z. 79: 459–466.
Fagerlind, F. 1947. Gyn€oceummorphologische und Swamy, B.G.L. 1960. Contributions to the embryo-
embryologische Studien in der Familie Olacaceae. logy of Cansjera rheedii. Phytomorphology 10:
Bot. Notis. 1947: 207–230. 397–409.
Fagerlind, F. 1959. Development and structure of the Swamy, B.G.L., Rao, J.D. (1963) 1964. The endosperm of
flower and gametophytes in the genus Exocarpos. Opilia amentacea Roxb. Phytomorphology 13:
Svensk Bot. Tidskr. 53: 257–282. 423–428.
Johri, B.M., Agarwal, S.J. 1966. Morphological and embry- Treub, M. 1881. Observations sur les Loranthacées. Ann.
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Quinchamalium chilense Lam. Phytomorphology Venturelli, M. 1981. Embriologia de Struthanthus vulgaris
15: 360–372. (Loranthaceae-Loranthoideae). Kurtziana 14:
Johri, B.M., Raj, B. 1965. Embryo sac development in 73–100.
Moquiniella. Nature 205(4969): 415–416. Zaki, M., Kuijt, J. 1994. Ultrastructural studies on the
Kuijt, J. 1967. On the structure and origin of the seedling embryo sac of Viscum minimum. II. Megagameto-
of Psittacanthus schiedeanus (Loranthaceae). Can. J. genesis. Can. J. Bot. 72: 1613–1628.
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Berkeley and Los Angeles: Univ. Calif. Press. sis. Protoplasma 185: 93–105.
Fruits, Seeds and Seedlings
Fruits. The fruits of Santalalean species are almost opmental history of this failure is not known. The
exclusively one-seeded. A rare, occasional excep- seedlings of the first two genera are strikingly
tion is seen especially in some Viscaceae, where massive, and make up their great bulk, having
two seedlings share a common endosperm. This is taken over the storage function of endosperm.
not surprising, as more than one embryo sac are As mentioned earlier, it is probably a common
usually present in each ovary. However, multiple feature in Loranthaceae that endosperm, where it
embryo sacs are also present in Loranthaceae and occurs, is compound, i.e., derived from the fusion
other families, where fruits with 2 embryos have nuclei of several embryo sacs, but this aspect
not, as far as I know, been recorded. needs better confirmation. Endosperm is usually
The majority of fruits in the order have a copious except perhaps in Ligaria; it is grooved in
fleshy surface layer, indicating dispersal by ani- Atkinsonia, Gaiadendron and Brachynema,
mals. A sclerified layer is frequent below that deeply so in Octoknemaceae and some Santalac-
softer one in Santalaceae, Olacaceae, and others. eous mistletoes (Kuijt 1990).
In the case of mistletoes, dispersal agents are In Cansjera, we find the additional complica-
birds and sclerified layers are absent, but the tion of certain endosperm cells developing elabo-
fruits of Tristerix corymbosus in southern South rate haustorial outgrowths (Swamy 1960). At first,
America are also eaten by a small marsupial, a single, superficial endosperm cell near the floral
Dromiciops gliroides (Amico and Aizen 2000), base grows downwards, becomes spindle-shaped,
the distribution of which seems to some extent and eventually develops (usually two) tubular
limited by that of the mistletoe (Rodrı́guez-Cabal extensions that ramify in a coral-like fashion.
and Branch 2011). The mistletoe Nuytsia flori- Several adjacent endosperm cells then go through
bunda is unique in having dry, winged fruits the same development, the ultimate branches
that may be wind-dispersed. mingling with those of the first cell. Clearly, this
The exact origin of the various layers of the system represents elaborate absorption equip-
fruit wall, however, has frequently not been ment supplying the differentiating endosperm.
detailed. The layer of viscin tissues in mistletoe The remarkable fact is that each of these hausto-
fruits presumably is derived from the innermost rial cells, notwithstanding its ramifications,
layer of the ovary wall; the origin of the peculiar remains uninucleate.
fibers in the fruit wall of Dendrotrophe and There is a special feature of endosperm in a
related genera also needs to be investigated. number of dendro-parasitic members of the
order that requires comment, i.e., the presence
Seeds. Endosperm is produced in the seeds of of chlorophyll. This feature has obviously evolved
Santalales throughout the order, with a couple independently in a number of taxa, and is of great
of exceptions. In the New World genera importance to sustain the growth of the seedling
Aetanthus, Psittacanthus, and Lepidoceras it in the early stages of its germination (and some-
fails to develop, but the relevant cellular or devel- times parasitic establishment). Green endosperm
22 Fruits, Seeds and Seedlings
in Viscaceae has been known for many years, (Hiepko 2008), Santalum album (Bhatnagar
but is also known for Misodendraceae (Kuijt 1965), and Urobotrya (Hiepko 2000). All these
1969) and Dendromyza, and, in Loranthaceae, in genera germinate hypogeously, as does Thesium.
Notanthera (J.K., pers. observ.), Lysiana exocarpi Cryptocotyly was illustrated for Ximenia by Mus-
(Brittlebank 1908), and Amylotheca dictyophleba selman and Mann (1977) but not mentioned in
(Bajaj 1970). the text. The primary root of Champereia, Ago-
nandra, Urobotrya (Hiepko 2000), Gaiadendron
Seedlings. As far as known, the great majority of (Kuijt 1963), Maburea (Maas et al. 1992), and
Santalales have two cotyledons; however, numer- Santalum (Pilger 1935) swells up significantly
ous genera are not known on this regard. Excep- upon establishment.
tions (in brackets) are seen in Opiliaceae (2–4,
usually 3), Coulaceae and Heisteria (3 or 4, rarely References
2); other Olacaeae and Schoepfia (2 or 3); Octo-
knemaceae (up to 6); Nuytsia (commonly 3); Amico, G., Aizen, M.A. 2000. Mistletoe seed dispersal by a
Psittacanthus (2, 3, or up to 11 in P. schiedeanus). marsupial. Nature 408: 929–930.
Phanerocotyly is the rule in the seedlings Bajaj, Y.P.S. 1970. Growth responses of excised embryos
of Santalales, but cryptocotylar seedlings have of some mistletoes. Zeitschr. Pflanzenphysiol. 63:
408–415.
evolved in numerous genera. In mistletoes, first Bhatnagar, S.P. 1965. Studies in angiospermous parasites.
of all, seedlings are cryptocotylar (and the No. 2. Santalum album – the Sandalwood Tree. Bull.
cotyledons apically connate) in numerous Old Nat. Bot. Gard. 112: 1–190.
Blakely, W.F. 1922–1928. The Loranthaceae of Australia.
World Loranthaceae, as well as in the New World Proc. Linn. Soc. New South Wales 47: 1–25, 199–222,
Tristerix. In T. aphyllus, the seedling forms a tor- 391–414 (1922); op. cit. 48: 130–152 (1923); op. cit.
pedo-shaped structure on which cotyledons are no 49: 79–96 (1924); op. cit. 50: 1–24 (1925); 53: 31–50
longer recognizable, and nearly the same is true for (1928).
Brittlebank, C.C. 1908. The life-history of Loranthus exo-
Lepidoceras peruvianus (Kuijt 1988). In a single carpi. Proc. Linn. Soc. N. S. Wales 33: 650–658.
species of Psittacanthus, P. sonorae, cryptocotyly Heckel, E. 1901. Sur le processus germinatif dans les
has also evolved, but the cotyledons remain sepa- genres Onguekoa [sic] et Strombosia de la famille
rate, as they do in Ligaria (Kuijt 1982), where the des Olacacées. Ann. Mus. Col. Marseilles 8: 17–27.
Hiepko, P. 2000. Opiliaceae. Flora Neotropica 82: 1–53.
cotyledons eventually emerge. A unique interme- Hiepko, P. 2008. Opiliaceae. Species Plantarum: Flora of
diate is seen in Desmaria, in which one cotyledon the World 12: 1–71.
remains in the endosperm while the other one Kuijt, J. 1963. On the ecology and parasitism of the Costa
emerges as a small foliar organ (Kuijt 1985). Atkin- Rican tree mistletoe, Gaiadendron punctatum (Ruı́z
& Pavon) G. Don. Can. J. Bot. 41: 927–938.
sonia may also be cryptocotylar (Blakely 1923/24). Kuijt, J. 1969. The biology of parasitic flowering plants.
Nearly all Viscaceae are phanerocotylar, even Berkeley and Los Angeles: Univ. Calif. Press.
though cotyledons are very small. Arceuthobium, Kuijt, J. 1978. Germination of Comandra (Santalaceae).
Phoradendron californicum, and Viscum mini- Madroño 25: 202–204.
Kuijt, J. 1982. Seedling morphology and its systematic
mum are exceptions in having scarcely recogniz- significance in Loranthaceae of the New World,
able cotyledons that do not emerge. In the latter with supplementary comments on Eremolepidaceae.
species, as well as in the (phanerocotylar) species Bot. Jahrb. Syst. 103: 305–342.
Kuijt, J. 1985. Morphology, biology, and systematic rela-
of the hyperparasitic Phoradendron dipterum tionships of Desmaria (Loranthaceae). Plant Syst.
complex, shoots emerge from an external disk Evol. 151: 121–130.
constituting the original haustorial disk. The seed- Kuijt, J. 1988. Monograph of the Eremolepidaceae. Syst.
ling of Misodendrum needs to be reinvestigated: a Bot. Monogr. 18: 1–60.
Kuijt, J. 1990. Correlations in the germination patterns of
closed, tubular envelope is said to enclose what Santalacean and other mistletoes. In: Baas, P. et al.
appear to be the first true leaves, and cotyledons (eds.) The plant diversity of Malesia, pp. 63–72.
do not seem to have been identified (Kuijt 1969). Maas, P.J.M., Baas, P., Boesewinkel, F.D., Hiepko, P.,
Beyond the mistletoes, cryptocotyly charac- Lobreau-Callen, D., Van den Oever, L., Ter Welle,
B.J.H. 1992. The identity of “Unknown Z”: Maburea
terizes Agonandra (Hiepko 2008, 2000), Coman- Maas, a new genus of Olacaceae in Guyana. Bot.
dra (Kuijt 1978), Ongokea (Heckel 1901), Opilia Jahrb. Syst. 114: 275–291.
References 23
Musselman, L.J., Mann, W.F. 1977. Cataphyll behavior in Rodrı́guez-Cabal, M.A., Branch, L.C. 2011. Influence of
Ximenia americana seedlings (Olacaceae). Beitr. habitat factors on the distribution and abundance
Biol. Pflanzen 53: 121–125. of a marsupial seed disperser. J. Mammalogy 92:
Pilger, R. 1935. Santalaceae. In: Engler, A., Prantl, K., Die 1245–1252.
nat. Pflanzenfam., 2nd edn, 16b: 52–91. Swamy, B.G.L. 1960. Contributions to the embryology of
Cansjera rheedii. Phytomorphology 10: 397–409.
Germination
The brief period between seed dispersal and con- based on negative phototropism, because
tact with living host tissues in mistletoes repre- when—as often happens—the seed adheres to
sents the only part of the life cycle that is the lower part of a branch, the seedling’s radicle
not dependent on the host. It is also a period of grows upwards. The process is entirely compara-
vulnerability to predation by animals and, in ble to that of the epiphytes Dischidia (Asclepiada-
many environments, to dehydration. Therefore, ceae) and Aeschynanthus (Gesneriaceae) where
we might expect rapid germination, and this the radicle undergoes a similar curvature, and
seems to be true for many tropical and subtropical where the disk-like root apex becomes anchored
species. However, seedlings in more temperate by means of a ring of fine hairs (Docters van
climates may be extremely slow in development, Leeuwen-Reijnvaan and Docters van Leeuwen
as is the case in Arceuthobium. Most seeds of 1913). However, in some Viscaceae the radicle
Loranthus europaeus and Viscum album also does not immediately show such a curvature but,
remain dormant until spring (Wiesner 1897). At instead, grows out parallel to, or along the host
least the seeds of Viscum album and V. cruciatum surface for some distance (Phoradendron califor-
have an absolute light requirement before germi- nicum: Kuijt 1989; Arceuthobium: Kuijt 1960).
nating. Eventually, the radicular apex touches the surface
The fact that (at least in tropical mistletoes) and expands to form a holdfast that secures last-
germination follows immediately upon dispersal ing contact. The seedling is thus geotropically
led to speculations that a germination inhibitor neutral under field conditions (Lamont 1983).
might be present in the fruit, as early suggested Adherence to the host is of two sorts. Initially
by Wiesner (1897). The strongest recent sugges- the seed is attached by the viscin that in many
tion to this effect has been made by Lamont species surrounds the seed or part of it, as in most
(1983), namely that predispersal dormancy is or all Viscaceae. Those seeds that have viscin only
maintained through high CO2 levels controlled at one end of the seed are able to influence the
by the impermeable fruit wall. A related sugges- direction of the subsequent radicle growth. How-
tion was previously made by Lamont and Perry ever, the forward surface of the radicle, usually
(1977) to the effect that the pericarp may restrict becoming disk-like, also secretes an adhesive that
oxygen entry into the embryo. Release upon dis- is used as counter force to the intrusive organ
persal is believed to be experienced by the apical when entering the host. The most elaborate secre-
meristem of the radicle that protrudes from the tive system of this sort is known from the curious
seed. polyp-like surface cells of Passovia pyrifolia.
In ramal mistletoes the radicle (sometimes These cells at maturity are extraordinary, polyp-
referred to as hypocotyl because it lacks a root like structures that form a massive layer, their
cap) usually curves quickly towards the substrate multiple slender arms tightly intermingled (Dob-
when germinating. This growth movement is bins and Kuijt 1974). The swollen tips of these
26 Germination
arms appear to burst, probably releasing an adhe- in their life-history. Beaufortia, Miscell. Publ. 4:
sive. This second adhesive often is strong enough 104–207.
Docters van Leeuwen-Reijnvaan, J., Docters van Leeuwen,
to allow the remnant of the endosperm and viscin W.M. 1913. Beitrag zur Kenntnis einiger Dischidia-
to be lifted away from the substrate, as shown by Arten. Ann. Jard. Bot. Buitenzorg III, 12: 65.
Doctors van Leeuwen for Macrosolen (1954, their Kuijt, J. 1960. Morphological aspects of parasitism in the
Fig. 21). dwarf mistletoes (Arceuthobium). Univ. Calif. Publ.
Bot. 30: 337–436.
Kuijt, J. 1989. A note on the germination and establish-
ment of Phoradendron californicum (Viscaceae).
References Madroño 3: 175–179.
Lamont, B. 1983. Germination of mistletoes. In: Calder,
M., Bernhardt, P. (eds.) The biology of mistletoes.
Dobbins, D.R., Kuijt, J. 1974. Anatomy and fine structure Sydney: Academic Press.
of the mistletoe haustorium (Phthirusa pyrifolia). Lamont, B., Perry, M. 1977. The effects of light, osmotic
I. Development of the young haustorium, II. Pene- potential and atmospheric gases on germination of the
tration attempts and formation of the gland. Amer. J. mistletoe Amyema preissii. Ann. Bot. 41: 203–209.
Bot. 61: 535–543, 544–550. €
Wiesner, J. 1897. Uber die Ruheperiode und u €ber einige
Docters van Leeuwen, W.M. 1954. On the biology of some Keimungsbedingungen der Samen von Viscum
Javanese Loranthaceae and the role birds play album. Ber. Deutsch. Bot. Ges. 15: 503–516.
Biological and Structural Aspects of Parasitism
Recognition of Parasitism in Santalales. The ear- In any case, it came as a complete surprise
liest realisation of the phenomenon of parasitism when Mitten (1847) found that Thesium linophyl-
in higher plants generally is difficult to pinpoint, lum in England was parasitic on the roots of
and this is true also in Santalales (Kuijt 1969) neighboring plants. At that time, it was thought
even though mistletoes were known to some to be a peculiarity of that particular species. It was
early observers. Theophrastus was aware of per- not until two decades later that Solms-Laubach
haps both common European species, Loranthus (1867–1868) produced the strong focus on the
europeus and Viscum album, as also reported by haustorium of parasitic flowering plants that has
Pliny (Tubeuf 1923). This does not mean, of laid the foundation for a rational view of parasitic
course, that the nature of parasitism was recog- plants. Before that time, the conception of para-
nized at that time. sitism was vague even in the minds of astute
It is very likely that an early administrator of naturalists like Charles Darwin and Alfred Russell
the Dutch East India Company, H.A. van Rheede Wallace (see their remarkably parallel statements
tot Draakenstein (1637–1691), was the first per- upon first seeing a tropical forest, as cited in
son to refer to parasitism in flowering plants. In Eisely 1979, p. 19 and Oldroyd 1980, p. 75). The
his Hortus Indicus Malabaricus (1678–1703), he distinction between non-parasitic epiphytes and
describes and illustrates a species of Scleropyrum lianas, on the one hand, and parasitic mistletoes,
of Santalaceae (“Itti-canni”, his Table XXIX). In on the other, was obviously not clear to them; it is
the accompanying description, he writes: “Nasci- particularly curious that Darwin never commen-
tur supra arbores ac Maravaras, continuo radices ted on Misodendrum, which is extremely conspic-
emittens incorticibus arborem, nunquam in uous in the area of the Beagle Channel and nearby
terra.” Dr. Roy Gereau of the Missouri Botanical inland areas. The fact that confusion persisted
Garden has kindly provided a translation: “It well into the 20th century in the minds of bota-
germinates [is borne] on trees and Maravaras nists is attested by the use of parasitism in the
[?], immediately putting forth roots into the naming of epiphytic plants such as Senecio para-
tree’s bark, never in soil.” It is difficult to know siticus Hemsley (Asteraceae; Hemsley 1881),
how to evaluate this statement. Scleropyrum, as a Agalmyla parasitica Kuntze (Gesneriaceae;
member of Santalaceae, is a root parasite even Kuntze 1891), and Parasitipomea formosana
though this was not documented until relatively Hayata (Convolvulaceae; Hayata 1916). For
recently (Nicolson et al. 1988). However, it is many years, the parasitism of the gymnosper-
known to be a terrestrial tree. In all probability, mous genus Parasitaxus (Podocarpaceae) was
the observation by Rheede tot Draakenstein is in not documented, but that has now been accom-
error, and is perhaps based on second-hand plished convincingly (Feild and Brodribb 2005).
information. Arnott (1838) also doubted its reli- At this time, numerous Santalalean non-
ability and, in contrast to Malécot et al.’s (2004) mistletoe genera have been shown to be parasitic
statement, did not document parasitism. (Tables 2 and 3).
28 Biological and Structural Aspects of Parasitism
Table 2 Documented Santalalean parasitism beyond mistle- the Santalalean haustorium were first fully out-
toes and Santalaceae, s.l lined (Barber 1906, 1907a, 1907b, 1907c, 1908),
Agonandra (Kubat 1989) Opiliaceae some 40 years after the pioneer work of Solms-
Cansjera (Barber 1908; Weber 1977; Hiepko Opilaceae
and Weber 1978)
Laubach (1867–1868). These complexities make it
Champereia (Kubat 1987) Opiliaceae clear that the evolution of parasitism must have
Lepionurus (Kubat 1987) Opiliaceae taken place over a very long time. The common-
Melientha (Kubat 1987) Opiliaceae alities of the organ in various families of Santa-
Opilia (Kubat 1987) Opiliaceae lales might suggest that parasitism has evolved
Olax (Barber 1907b) Olacaceae
Ptychopetalum (Anselmino 1933) Olacaceae
once only in the order.
Rhopalopilia (Kubat 1987) Opiliaceae Some families (Aptandraceae, Coulaceae, and
Schoepfia (Werth and Baird 1979) Schoepfiaceae Octoknemaceae) so far appear to be entirely
Urobotrya (Kubat 1987) Opiliaceae autotrophic1 (Teo 1997), even though suspicions
Ximenia (Barber 1907c; DeFilipps 1969) Ximeniaceae linger even there. Octoknemaceae in Nickrent
Not yet known to be parasitic:
Aptandraceae, Coulaceae,
et al. (2010) are presumed to be parasitic because
Octoknemaceae, “Strombosiaceae” of their position in a consensus phylogeny (as are
Suspected of parasitism in Malécot et al. (2004): Anacolosa, Aptandraceae), but no documentation of this fact
Aptandra, Cathedra, Chaunochiton, Curupira, Douradoa, is available (Gosline and Malécot 2012). In
Dulacia, Harmandia, Malania, Ongokea, Phanerodiscus Schoepfiaceae, the single genus, Schoepfia, is
known to be parasitic (Werth and Baird 1979);
in the eleven genera that Nickrent et al. (2010)
assign to Opiliaceae, only Cansjera at first had
Table 3 Documented parasitism in woody, terrestrial Santa-
laceae, s.l. (woody African species of Thesium are undoubt- been clearly documented in the early work of
edly also parasitic, as are their herbaceous congeners) Barber (1908), but Kubat’s work (1987) raised
Anthobolus (Stauffer 1959) the total to eight genera; in Ximeniaceae, parasit-
Acanthosyris (Barroso 1969) ism is known for Ximenia itself but not yet for the
Buckleya (Piehl 1965b) other three genera (Barber 1907c; DeFilipps
Colpoon (Visser 1981)
1969), and two of the three genera placed by
Daenikera (Kuijt 1990).
Exocarpos (Stauffer 1959) Nickrent et al. (2010) in Olacaceae (Olax and
Nestronia (Piehl 1967) Ptychopetalum) are known to be parasites (Bar-
Okoubaka (Swaine and Hall 1986; Veenendaal et al. 1996) ber 1907b; Anselmino 1933). In Okoubaka and
Osyris (Pizzoni 1906) Acanthosyris there have been earlier field obser-
Pyrularia (Leopold and Muller 1983)
vations suggesting parasitism; both cases have
Santalum (Barber 1906, 1907a)
Scleropyrum (Nicolson et al. 1988) now been documented (Barroso 1969; Nee 1996;
Spirogardnera (Stauffer 1968) Veenendaal et al. 1996). Caution is warranted in
referring to apparently non-parasitic taxa in San-
talales, especially for those related to proven par-
Since the phenomenon of parasitism is cen- asitic ones. In those cases, the complexity and
tral in the systematics of Santalales, it is regretta- sophistication of haustoria makes it difficult to
ble that its evolutionary origin in the order believe that parasitism would have evolved in two
remains completely hidden from us. Clues to its genera but not in the remaining taxa. If it can be
origin might have been expected to exist in a proven that a non-parasitic species is closely
greater simplicity of the parasitic organ (hausto- related to a parasitic one, this raises the possibility
rium) of members that are generally thought to either that parasitism has evolved more than once,
be more basal in the order, such as Olacaceae and or that it may be lost in some species (the latter is
Opiliaceae (Nickrent et al. 2010), but it is pre- denied as a likelihood by Malécot and Nickrent
cisely there that the profound complexities of 2008). It must be remembered that a demonstra-
1
The term “autotrophic” is not to be equated with “photosynthetic”, as numerous parasites in Santalales and elsewhere are
photosynthetic but not (entirely) self-nourishing.
Biological and Structural Aspects of Parasitism 29
tion of parasitism (i.e., the existence of haustoria) (ramal) parasitism. The situation in some of the
is often a difficult and time-consuming matter, Asiatic Santalaceous genera that parasitize host
especially if trees or large shrubs are targeted. branches remains unknown; especially in the
Much remains unknown about parasitism in highly advanced genus Phacellaria, but perhaps
Santalales, as is true for parasitic flowering plants also in Dendromyza and relatives, the presence of
generally. It is regrettable, for example, that the primary haustoria may be suspected, almost cer-
functional capacities of those roots of Santalalean tainly so exclusively in the former genus (Kuijt
root parasites that do not bear haustoria remain 1990). Secondary haustoria develop laterally
completely unstudied. Do they function like the from secondary roots, and are standard equip-
roots of autotrophic plants? If so, considering ment of root-parasitic members of Santalales as
that all such plants contain photosynthetic pig- well as in many Loranthaceous genera (Fig. 2),
ments, how long can root-parasitic members live especially (but by no means exclusively) in the
(or even reproduce) autotrophically? The answer New World as well as in a few Santalaceous
for Nuytsia is at least a year (Main 1947), for genera of branch parasites.
Gaiadendron punctatum at least 6 months (Kuijt In the following brief account of the struc-
1969). Root hair formation seems to be at a mini- ture of Santalalean haustoria it must be remem-
mum in such roots, particularly, after haustoria bered that it rests on definitive work only in
become functional (Pilger 1935), whereas root Cansjera, Exocarpos, Olax, Ximenia, Comandra,
hair formation is completely absent, for instance, and Passovia (Kuijt 1965a), with supporting indi-
in the three primitive, terrestrial mistletoe genera cations in Struthanthus (Kuijt 1971) and Schoep-
(Atkinsonia, Gaiadendron, Nuytsia). If so, how fia (Werth and Baird 1979). Similar haustoria are
does their functioning relate to that of haustoria? said to exist in several other genera by Kubat
What is the precise tissue path of nutrients taken (1987), and in Agonandra by Kubat (1989). How-
in? Several unsolved questions arise from the ever, since these studies represent a broad spec-
complex Santalalean haustorium itself. trum of families, we may assume that the general
Separately, the longevity of secondary haus- development sketched applies to at least the
toria themselves has been recorded in only a majority of parasites in the order. This refers to
few instances. They mostly remain alive and func- the early phases before entry takes place; at that
tional for one year or so (Pate et al. 1990a, 1990b; point significant diversity may follow. Specific
Fineran 1991). Rarely do they live for 10 years or peculiarities will be discussed in the appropriate
more (Buckleya, Kusano 1902; Exocarpos bidwil- families. The relevant studies are based on pri-
lii, Fineran 1963). The primary haustorium of mary haustoria (except for the species that lack
mistletoes, of course, normally lives as long as them), the others on secondary ones.
the plant itself, unless secondary ones function- The essential structure of the Santalalean
ally replace it, as happens rarely, e.g., in Peraxilla haustorium is as follows, even though the exter-
tetrapetala (Fineran 2001) and Desmaria mut- nal shapes of secondary and primary haustoria
abilis (Kuijt 1985). often differ (see Fig. 2). It tends to have a globu-
lar, disk- or saddle-shape, and is initially made up
Haustoria in Santalales.2 Haustoria in Santalales of undifferentiated parenchyma except for a
may be either primary or secondary. Primary clearly defined epidermal layer. At an early
haustoria develop directly from the radicular stage, when the haustorium becomes attached to
pole of the seedling and are, as presently known, the host organ, a concentric layer of crushed cells
limited to Eremolepidaceae, Misodendraceae, (a collapsed layer) appears in the outer regions.
Viscaceae, and all Loranthaceae except Atkinso- Somewhat later, a group or (at least sometimes
nia, Gaiadendron, and Nuytsia (root-parasitic double) plate of cells in the lower center is seen to
genera having secondary haustoria only). In become prominent, especially through its dense
other words, the primary haustorium in the staining qualities. The cells in the middle of this
order represents an adaptation to arboreal cluster or plate slowly withdraw their cellular
2
The term haustorium was introduced by A.P. de Candolle (1813) when discussing Cuscuta (Convolvulaceae).
opment. Direct contact with the vascular system

of the host is usually secured, apparently only
with the xylem. This may take the form of a
partial encirclement of the latter’s stele. In mis-
tletoes, the tip of radial haustorial structures is
apparently stopped by the secondary xylem of the
host, which continues to be added to, thus invest-
ing that portion of the endophyte. Differentiation
of the parasite’s xylem ensures some lasting
xylem-xylem continuity. The physiological
aspects of this elaborate process of entry are
entirely unknown; no enzymatic substances
have been demonstrated in any haustorial struc-
tures except for an indication of acid phosphatase
in the endophyte of Comandra (Toth and Kuijt
1977). It is possible that a gland is not formed in
Viscaceae, as discussed under that family.
In many Loranthaceae, the host reacts by
forming a woody placenta-like cup to support
the maturing haustorium. This cup is usually
elaborately grooved in a radial fashion. Since the
Fig. 2. Sectional diagram of young Santalalean hausto- haustorial tissue is less dense than the adjacent
rium prior to penetration of host. A Collapsed zone, B host xylem, it may fall away after death, leaving
meristematic area generating intrusive organ, C gland, H the so-called woodrose exposed (Fig. 3). Such
host. (Original J. Kuijt)
structures in several parts of the tropics are fre-
quently sold (and mostly misinterpreted) for the
contents away from each other, a transformation tourist trade. Especially those from Southeastern
that eventually leads to the collapse of the thin Asia are often embellished with finely carved ani-
cell walls separating them. In this way, a lysigen- mal representations. This trade may locally result
ous cavity is formed called the gland that is filled in a sharp decline in mistletoe populations, as
with unknown substances and cell remnants. woodroses take many years to develop.
Immediately proximal to (above) the gland, a
compact meristematic cluster of cells is differen- Tissue Continuity with the Host. The eventual,
tiated. The intrusive organ takes its origin from mature haustorial connection is often primarily
this meristematic center. It traverses the gland, a parenchymatous interface, xylem continuity
breaks through the intervening superficial haus- existing but being less prominent. This was well
torial tissue, and attempts to enter the host. How- demonstrated for Olax by Pate et al. (1990a; see
ever, its effort to gain entry may not be at first also Kuo et al. 1989), but also has been evident in
successful. If it is not, it flattens out against the several earlier studies of the endophyte of Visca-
host and enlarges. A new gland forms in the ceae (Kuijt 1960; Calvin 1967). Most of the inter-
center of this enlarged parenchymatous mass, face consists of parenchyma; Calvin (1997)
along with a new intrusive organ, and a new reports that this is so for 71 % of the host and
invasion attempt is staged. This may apparently 95 % of the parasitic interface in a Phoradendron-
be repeated several times. Thus, an older hausto- Juglans combination. Nevertheless, transfer of
rium may have several concentric shells or lobes materials through open xylem-xylem connections
indicating past attempts at host entry. However, that frequently form may well be more produc-
the several collapsed zones associated with them tive, or may introduce different types of materials
are not all necessarily related to attempted into the parasite, and the more extensive paren-
entries. chyma interface is not necessarily more efficient.
If entry is affected the endophyte, as indicated The haustorial interface of Psittacanthus (and
earlier, may take very different courses of devel- perhaps many other Loranthaceae) seems to
Fig. 3. Woodroses caused by the mistletoe Psittacanthus as seen from above, the mistletoe tissues having fallen
sp. A Young woodrose on a Mexican member of the away. (From Engler 1889, who erroneously interpreted
Salicaceae as seen from below; several branches of the them as caused by a sp. of Phoradendron; drawn by
parasite visible behind. B Large woodrose on a legume J. Tegetmeyer)
consist of mostly xylem, the interface cells of the Arceuthobium, also, a low level of photosynthesis
mistletoe approaching the host xylem perpendic- prevails (Hull and Leonard 1964a, 1964b), but no
ularly (Kuijt and Lye 2005). phloic bridge exists. Even true holoparasites in
other families may not have a phloem connec-
a. Xylem continuity. It is exceedingly difficult to tion, as in Boschniaka (Orobanchaceae: Toth and
obtain a quantitative appraisal of the degree to Kuijt 1985). Even if no direct phloem continuity
which xylem continuity exists across a parasitic exists, however, the withdrawal of materials from
interface. In fact, it is only in Olax that an approx- host phloem transmitted through parenchyma
imation has been made (Pate et al. 1990a, 1990b). remains a possibility.
As mentioned above, the most massive of such a c. Other features. Two unusual and unexplained cell
xylem bridge would seem to be present in the types have been discovered in the haustoria of
woodroses in Loranthaceae (Kuijt and Lye mistletoes and others. Graniferous tracheary ele-
2005). In this context, it is important to remem- ments of at least two types are known from the
ber that a significant (sometimes seasonally vari- haustoria of several groups, including some mis-
able) amount of organic material is known to be tletoes, Exocarpos (Fineran et al. 1978; Fineran
present in host xylem. 1979; Fineran and Bullock 1979), Opilia (Fineran
b. Phloem continuity? The physiology of one squa- 1985), Olax (Fineran et al. 1987), and Cansjera
mate mistletoe, Phoradendron californicum, has (Weber and Hildebrand 1978). Flange cells (an
led to it being referred to as a “phloem-feeder” unusual, transfer-like cell type) have been
(Ehleringer et al. 1985), and Tristerix aphyllus has described in both Korthalsella and Phoradendron
been called a holoparasite (Kraus et al. 1995), but (Fineran 1996, 1998; Fineran and Calvin 2000).
a parasitic connection to the host phloem has not They represent an enigmatic cell type with com-
been demonstrated in any member of Santalales. plexly structured walls, and are commonly asso-
In any case, a low level of photosynthesis (or even ciated with xylem. They have been described for a
its absence) does not allow any inference on vas- few non-parasitic plants as well, but in the two
cular connections between the two partners. In last genera mentioned above are known only
from haustorial tissues. There they appear to be path of transfer involved the parasite’s xylem at
associated with events subsequent to materials the interface. More recently, this view has been
being moved from the host across the interface. challenged in several Santalalean parasites. The
In Phoradendron leucarpum regular transfer focus thus has shifted to the apoplastic contin-
cells, in association with flange cells, are present uum involving the walls of parenchymatous
in the sinkers themselves (Fineran and Calvin interface cells, from which further distribution
2000). Graniferous tracheary elements of various to the parasite’s more remote parts occurs. The
sorts have also been demonstrated in non-Santa- convoluted plasmolemma and its differentiation
lalean parasites. into plasmotubules near the interface appear to
confirm this view (Coetzee and Fineran 1987).
Uptake of Water and Nutrients from the Host. Photosynthetic pigments are present in all
Among Santalalean root parasites, Pate and cow- mistletoes, and the great majority are colored
orkers have dealt with the parasitism of Olax bright green, even though Tristerix aphyllus and
phyllanthi in considerable detail (Kuo et al. (probably seasonally) Psittacanthus nudus as well
1989; Pate et al. 1990a, 1990b). Ninety-nine per- as numerous species in the related Viscaceae are
cent of the cellular host-parasite contact in this leafless. No modern physiological work has been
species consists of parenchyma tissue, and there done on such aspects, however, even on species in
is no lumen continuity between partners. In San- the temperate areas of the world where the
talum album, lumen to lumen continuity is prob- required facilities are generally better.
ably also lacking entirely (Radomiljac et al. 1998). As mentioned elsewhere, there are no Santa-
Nevertheless, a substantial intake of xylem N by lalean holoparasites. Chlorophyll concentrations
the parasite occurs from several legume hosts, but are low in some taxa like Arceuthobium and Tris-
little from the non N-fixing host Eucalyptus terix aphyllus; in at least some leafy mistletoes, in
camaldulensis. An apoplastic pathway of water contrast, the concentration of leaf chlorophyll
uptake is therefore indicated (as also shown for appears to be roughly the same as that of the
the mistletoe Korthalsella by Coetzee and Fineran host (Hull and Leonard 1964b). The question of
1987). Deep-rooted and shallow-rooted hosts photosynthesis in mistletoes, however, must be
apparently correspond to different conditions in seen in relation to the intake of water and nutri-
the parasite. Santalum album shows superior ents from the host. It is crucially important to
growth performance and higher photosynthetic know what materials are taken from the host.
rates and foliar N concentrations when partnered Modern analytical methods have demonstrated
with legumes rather than Eucalyptus. that NH4 and organic nitrogen are important in
A different study was carried out by Fer et al. this respect (Lamont 1983). It is not clear whether
(1993) on the parasitism of Thesium humile on this uptake is done actively or passively; a combi-
Triticum, where it was shown that sucrose nation is likely. Mineral concentrations, espe-
absorbed from the host is rapidly converted to cially of K, tend to be much higher in mistletoes
mannitol. The latter also seems to be the end than in their hosts (Lamont 1983, 1985; Panvini
product of the parasite’s own photosynthesis. and Eckmeier 1993; paradoxically, Bowie and
The structural details of the haustorial inter- Ward 2004 have found the opposite to be true in
face form a necessary backdrop to any considera- Plicosepalus in the Negev Desert). Whereas Mar-
tions dealing with movement of host materials shall and Ehleringer (1990) concluded that the
into the parasite. The essential facts here are (1) mistletoe they studied obtained 60 % of its assim-
the bulk of the contact between partners consists ilates from the host, it must be pointed out that
of parenchyma; (2) xylem-xylem contact is this mistletoe was a squamate species, and that
known in most but not all cases, and tends to be this figure may be radically different for leafy
minimal even though sometimes open; (3) there species. Moore (1994) reports that, for a leafy
is no direct contact of parasitic cells with host species, roughly 15 % of the total carbon gain is
phloem; and (4) there is no evidence of plasmo- derived from the xylem stream of the host. That a
desmal continuity across the haustorial interface. substantial transfer of host carbon must take
A long-standing tradition, in the case of chloro- place along with the transfer of organic nitrogen
phyllaceous parasites, has been that the main is now an accepted aspect of mistletoe physiology
(Raven 1983). This is associated with high tran- tical roots, as in Notanthera heterophyllum (Kuijt
spiration rates that tend to be substantially higher 1989) and some others in Australia (Barlow 1971)
in mistletoes as compared to their hosts. For and Africa (Calvin and Wilson 1998); very rarely,
example, Johnson and Choinski (1993) found even inflorescences may emerge from them (Kuijt
that the parasite’s transpiration rates (daylight) 1981). Especially in Struthanthus and some spe-
were approximately twice as high in Tapinanthus cies of Passovia, young leafy shoots may also pro-
as compared with those of its hosts (see also duce epicortical roots with haustoria, sometimes
Davidson et al. 1989; Panvini and Eckmeier resulting in an impenetrable covering by the para-
1993). The unusually high transpiration rates of site’s branches on the tree’s crown. Struthanthus
mistletoes may provide a mechanism to acquire orbicularis is especially noteworthy in this regard,
nitrogen (Ehleringer et al. 1985). However, having young leaves in the shape of grappling
Bannister et al. (1999) and Bannister and Strong hooks with thigmotropic petioles capturing solid
(2001) have recorded different conditions in New structures, the nearby stem quickly forming
Zealand mistletoes, cautioning us not to extrapo- epicortical roots and haustoria (Kuijt 1964). In
late views between taxa uncritically. Tripodanthus flagellaris, epicortical roots emerge
It is an unfortunate fact that precise struc- only in pairs at the nodes (Kuijt 1982). Its conge-
tural and chemical details of the mistletoe-host ner, T. acutifolius, gives rise to masses of roots at
interface remain out of reach at present. All mate- the site of injury or pressure by other organs (Kuijt
rials present in the parasite must have crossed 1989). Epicortical roots are absent from Misoden-
this boundary. Paradoxically, there have been draceae and Viscaceae, being found only in some
suggestions of this boundary representing a genera of Eremolepidaceae, Loranthaceae, and
major point of resistance to water uptake by the Santalaceae. In all likelihood they have evolved
parasite (Davidson and Pate 1992). As stated by independently in these three families, possibly
Davidson et al. (1989), “Much more must obvi- more than once in Loranthaceae.
ously be learned of the ultrastructural features of The primary haustorium, being the product
the mistletoe haustorium before . . . suggestions of the radicular apex of the seedling, undoubtedly
can be further tested.” represents an advanced development. This is also
indicated by its absence in the three most basal
Epicortical Roots. Epicortical roots bearing sec- genera of Loranthaceae, Atkinsonia, Gaiaden-
ondary haustoria are conspicuous features of dron, and Nuytsia. In the mistletoes, it is a
many mistletoe genera, both in the New World specific adaptation to ramal parasitism that
and the Old World (Calvin and Wilson 2006). In makes it impossible to attack host roots. In this
Viscaceae, green cortical strands sometimes are connection, it is interesting to speculate on the
exposed through the action of the host’s cork situation in the ramal parasites among Asiatic
cambium (Kuijt 1964), but are not to be compared Santalaceae. At least some Dendrotrophe species
to epicortical roots, which mostly originate from have evolved haustoria-bearing epicortical roots
the external base of the plant, just above the pri- from branches, the tips being lodged in branch
mary haustorium, and have an uncanny ability to crevices of the host (Kuijt 1990). The most
grow in the length direction of the host branch, remarkable genus in this group is Phacellaria,
especially proximally. While this latter preference which lacks epicortical roots but almost certainly
may have a physiological basis—the “upstream” has evolved a primary haustorium, perhaps the
haustoria, tapping the host’s incoming xylem only one in Santalaceae. Unfortunately, conclu-
stream, may be more functionally successful than sive evidence for this is not available.
others—it also has the incidental advantage in Some evidence has emerged that the host
rescuing those mistletoe seedlings that happen to species in some instances may determine whether
germinate on host leaves or small lower branches. a mistletoe is able to produce epicortical roots or
The most dramatic instances of this rescue effort not. The common neotropical mistletoe, Oryc-
can often be seen in Desmaria (Kuijt 1985), where tanthus alveolatus, in a Colombian locality pro-
secondary haustoria may become anchored in the duced such roots on some trees, but on
crevices of mature host trunks. It is uncommon to Euphorbia latazi there was no evidence of them
find vegetative shoots being produced by epicor- in either juvenile or mature stages (Kuijt 1989).
Instead, the primary connection became sur- further east (Barlow 1971), including the New
rounded by a massive ringwall of host tissues Zealand Ileostylus micranthus (Kuijt 1969).
about 5 cm in diameter. A similar instance is Among terrestrial Santalalean parasites, there
reported in Dendrophthoe by Hamilton and Bar- are many examples of shoot formation from
low (1963). This is different from developments underground organs, including Exocarpos (Stauf-
in Antidaphne viscoidea where old plants may fer 1959), Nuytsia (Herbert 1918–1919), and
also lack epicortical roots. In that case, juvenile Atkinsonia (Watson 2011). Among herbaceous
plants always produce epicortical roots with con- genera, Comandra and Geocaulon provide addi-
spicuous secondary haustoria but, as the plant tional examples.
ages, the tips of the roots with their haustoria
degenerate while the massive primary hausto- Host Preferences. The question of host prefer-
rium eventually unites with the nearest secondary ences in parasitic plants turns out to be a very
haustoria and root portions (Kuijt 1964). slippery subject (Kuijt 1979). In the vast majority
Anatomically, epicortical roots are anoma- of parasites in the Santalales, there are no reliable
lous, at times giving rise to some doubts (Thoday data, at least at the lowest taxonomic levels, and
1960) as to whether they truly are roots (the we must make do with anecdotal information
primary structure of the roots of the terrestrial based on field observations that often lack reli-
Atkinsonia, Gaiadendron and Nuytsia is clearly able documentation. For practical reasons, host
root-like even though lacking root hairs and preferences or host ranges are difficult to estab-
endodermis: Kuijt 1965b; Hocking and Fineran lish in terrestrial parasitic members of the
1983). The root cap, while present, is exceedingly order, even where such tendencies may exist.
thin, and root hairs are absent. (Venturelli 1984 Exceptionally, Werth and Baird (1979) were able
claims that a root cap in Struthanthus vulgaris is to establish that Schoepfia may have haustoria
absent, but her Fig. 1 leaves some doubts.) The on ten different host species from eight different
apical meristem certainly consists mainly of con- families. The seeming limitation to certain hosts
centric layers of cells, and neither an endodermis often may be based on the local predominance of
nor root hairs are present. In my own work on a susceptible hosts, as this can easily convey the
related species, I have also observed a parenchy- impression of limitation to such a host species.
matous central pith and lack of bundle structure. For example, Buckleya distichophylla has fre-
Epicortical roots, even though endogenous in quently been said to prefer Tsuga, but Piehl
origin, thus have some stem-like anatomical fea- (1965b) has shown that this co-occurrence is,
tures. instead, due to similar site preferences of parasite
and host. Careful scrutiny often reveals that other
Vegetative Reproduction in Santalales. Vegeta- species can also occasionally be attacked. Parallel
tive reproduction from roots or the endophyte early views on the parasitism of Pyrularia also
has evolved in various parts of the order, even turned out to be mistaken, as the species may
in ramal (aerial) mistletoes. The most dramatic parasitize at least 63 species of hosts belonging
instances of this are seen in Arceuthobium and in to 50 genera and 31 families, including ferns and
Viscum minimum, as detailed in Viscaceae, but gymnosperms (Leopold and Muller 1983).
other cases from endophytic portions are found Even in mistletoes, the situation may be more
in Dendrophthora and Phoradendron, too. Clonal complicated than locally meets the eye. A com-
reproduction from epicortical roots has emerged mon host in one area may turn out to be merely a
in several genera of Loranthaceae, sometimes secondary one in a different locality, as seems to
occurring rarely, as in Dendropemon and Oryc- be the case in Phoradendron leucarpum in the
tanthus (Kuijt 1976, 2011), but sometimes as a eastern United States. The reasons for such differ-
regular feature, as in Notanthera (Kuijt 1989) and ences escape us. In species seemingly restricted to
very dramatically from the endophyte in Tristerix one host, we often find rare, unexpected “jumps”
aphyllus and T. corymbosus (Kuijt 1988b). In the to another. As an example, Arceuthobium amer-
Old World, it has evolved in three African genera icanum, in the Alberta Rocky Mountains and
(Calvin and Wilson 1998) and in several genera British Columbia restricted to pines, very rarely
infects Picea engelmannii (Kuijt 1960) and other A somewhat different situation is encoun-
species in that genus, and this has been confirmed tered in the Phoradendron species centered
elsewhere (Hawksworth and Wiens 1996). Ameri- around the common P. dipterum. It is not clearly
can records from the genus are rife with conifer- established whether hyperparasitism on other
ous host names, but in no case do they indicate Viscaceae is their exclusive mode of life; some
exclusive limitations. Nevertheless, the genus has uncertainty remains, as situations in the field
never been recorded from anything but conifers. may be deceptive. In any case, here is a cluster
Beyond Arceuthobium, we can list several of species, rather than a single one, that have
instances of “near” host specificity. Misodendrum adopted the hyperparasitic mode of life. The
parasitizes Nothofagus spp. nearly exclusively; most striking species of this group is the curious,
rare instances on Aristotelia maqui and Caldclu- rare Mexican Phoradendron iltisiorum on Clado-
via paniculata are reported (Orfila 1978). Eubra- colea.
chion and Lepidoceras are known nearly entirely The genus Phacellaria has so far been
from Myrtaceae (Kuijt 1988a, Appendix, p. 56). collected only on fellow-Santalalean parasites in
From an evolutionary point of view, rare transfers Loranthaceae and Viscaceae (Danser 1939). The
may well be very important “trial extensions” of origin of such mistletoe hyperparasitism is to be
the host range. Nevertheless, certain mistletoe looked for in the feeding behavior of birds feed-
taxa show a level of host specialization that ing on a variety of mistletoe species. Nearly all of
appears to be absolute. Tristerix aphyllus has the above comments, of course, are focused on
never been found on anything but Cactaceae; the directly visible parasitism of mistletoes; for
Viscum minimum in southern Africa is known obvious reasons, comparable data for root-para-
to parasitize only fleshy Euphorbiaceae (Heide-- sitic terrestrial parasites are much more difficult
Joergensen 2008). As mentioned, Arceuthobium to ascertain. A special case of hyperparasitism
records on flowering plants do not exist; in fact, (also frequently found in terrestrial parasitism)
some species are found exclusively on Cupressa- is given where the parasite produces haustoria on
ceae, others on Pinaceae, but never both. Barlow its own organs; it simply means that it is unable to
and Wiens (1977) state that 75 % of Australian recognize the difference. The phenomenon is
mistletoes of open forest and woodland are host- often observed in neotropical genera with epicor-
specific. tical roots like Struthanthus and Passovia.
On the other hand, there are well-established
instances of very large numbers of hosts in cer- Amphiphagy? The question whether a parasite
tain parasitic Santalales, such as Viscum album can attack either the roots or the stems of the
(Tubeuf 1923) and Dendrophthoe falcata, the host is relevant to several Santalalean parasites,
latter with nearly 350 known host species but points to serious problems in the understand-
(Narasimha and Rabindranath 1964). Barber ing of the germination and host establishment or
even more than a century ago (1907a) registered attachment of such plants. We must be certain of
160 host species for Santalum album. the initial parasitic establishment site, whether
stem or root. In the two Loranthaceous instances
Hyperparasitism. A totally different phenome- mentioned by Nickrent et al. (2010) we read of the
non, of course, is the evolutionary specialization amphiphagous condition in “various species of
requiring certain other parasites as hosts. There Tripodanthus and Helixanthera” (Loranthaceae).
are examples of this especially in Viscaceae: Vis- In Tripodanthus acutifolius (Kuijt 1989) and in
cum loranthicola exclusively on various genera of Helixanthera, the structure of seedlings dictates
Loranthaceae, and other Viscum species similarly that they can become established only on host
parasitic on other mistletoes in tropical Asia; aerial host organs, not under subterranean con-
Dendrophthora epiviscum in the Caribbean on ditions, and this has been confirmed for the for-
other Dendrophthora and Phoradendron. Phacel- mer. In T. acutifolius, root parasitism does indeed
laria also is entirely limited to loranthaceous or occur, but is strictly secondary. Initial establish-
viscaceous mistletoes; the same seems to be true ment can occur only on host branches (or per-
for Phthirusa hutchisonii. haps very rarely on exposed roots). The profusion
of subsequently formed epicortical roots means where it was attached in only one place (which
that, especially on smaller hosts, such roots may sounds like a primary haustorium!); but else-
eventually reach soil level where they are fully where it was observed as a root parasite. Hambali
able to follow host roots underground and pro- (1977) makes parallel suggestions for Dendro-
duce functional haustoria. Plants of this species trophe varians in South Borneo. It is precisely in
may thus have haustoria on host roots and host such ecological conditions that exposed host
stems simultaneously. The nature of viscin, and roots might occasionally support what is basically
the structure and behavior of the primary haus- a branch-parasite; once again, better information
torium are such that T. acutifolius cannot become is needed. The separation between terrestrial and
established on host roots unless these are exposed epiphytic habitats in moist tropical areas is often
(as is often the case under tropical conditions). In unclear or nonexistent. The problem is high-
the paleotropics, Amyema species have been lighted by the occurrence in either a terrestrial
described similarly (Heide-Joergensen 2008), as or epiphytic position of Gaiadendron punctatum
has Helixanthera (Nickrent et al. 2010), but the (Kuijt 1963, 1989) that, erroneously, is equated
critical field observations are again lacking. We with amphiphagy in Malécot and Nickrent
must assume that such mistletoes are essentially (2008). The habit of Exocarpos pullei as reported
branch-parasitic. by Lam may well be comparable, and would not
Are there truly amphiphagous Santalalean amount to real amphiphagy. Surely the extremely
parasites elsewhere, i.e., ones that can start their rare occurrence of an Arceuthobium species on
existence on either stems or roots? Daenikera and an exposed pine root (see Hawksworth and
Spirogardnera are quite possibly the best candi- Wiens 1996, p. 14 and Fig. 2.14) does not make
dates (H€ urlimann and Stauffer 1957; Stauffer it amphiphagous. It should be added that there is
1968). In Spirogardnera (Stauffer 1968), the a single report describing a plant of Exocarpos
author leaves no doubt that it is a root parasite; parasitic on the stem of Eucalyptus (Coleman
Daenikera is said to be a root parasite on Myodo- 1934). It probably represented a rare case of a
carpus fraxinifolius (see Kuijt 1990). However, seed germinating in a moist crevice and establish-
as mentioned earlier, the initial attachment of a ing a functional haustorium.
parasite seedling to a host branch presupposes We know essentially nothing about the sti-
highly specialized tissues such as viscin cells muli needed for haustorial initiation in Santalales
(Gedalovich and Kuijt 1987) and the remarkable except that, in all probability, aerial parasites do
surface cells generated by the radicular epidermis not depend on stimuli from the host. Conditions
in Passovia (Dobbins and Kuijt 1974), tissues that of moisture and temperature being appropriate,
are useless when germinating under ground. such parasites germinate almost anywhere, even
Therefore, we urgently need to know the early on a sterile glass plate (Passovia pyrifolia). In
life history of the seedlings of such plants before Comandra, I have found profuse haustoria on a
we can evaluate this question. What are the struc- piece of buried plastic, but excavation shows
tural and developmental adaptations that would many haustoria to be formed precisely where
facilitate such a dualistic behavior, allowing encountering host roots. Kubat (1989) found
establishment under aerial as well as subterra- numerous Agonandra haustoria on the inside of
nean conditions? The question derives more a flowerpot.
importance from the suggestion by Nickrent
et al. (2010) that the ancestry of Viscaceae may Facultative Parasitism? In the general literature
have been amphiphagous. of flowering plant parasitism, the question of
The other references to amphiphagy that I facultative parasitism has been raised repeatedly,
know lack substantial data. Stauffer (1959) speaks but this is not so in Santalales except for the
of Exocarpos pullei as “Stamm- oder Wurzelpar- erroneous report by Holm (1924) who claimed
asit” but this appears to be based only on some that the mature plant of Comandra umbellata is
casual statements by Lam (1945). In the latter autotrophic while the juvenile one is parasitic. It
publication E. pullei is described in the protolo- seems to be generally accepted that within the
gue as a shrub growing in a rich, humid forest, order a species is parasitic or not but cannot in
attached to a branch of one of the tallest trees, the last analysis function in both modes; one
exception may be Ximenia about which Sleumer generally, and is relevant for some members of
(1984, probably erroneously) writes that its para- Santalales, too. That holoparasites exist, as in
sitism is facultative. Other, casual statements some Orobanchaceae, is beyond question—in
have appeared in the literature (e.g., Press et al. fact, entire families of holoparasites exist, as in
1991) to the effect that facultative parasites exist Lennoaceae and Rafflesiaceae (Kuijt 1969; Heide-
in flowering plants, but these remarks are insub- Joergensen 2008). Holoparasitism in plants that
stantial. The degree of dependence on the host have haustoria is usually defined in terms of the
has given rise to some speculation, but in Santa- total absence of chlorophyll. However, there are
lales only in the mistletoes. Such speculation has numerous parasitic plants that have, or seem to
largely been based on either the perceived reduc- have, significantly reduced amounts of chloro-
tion in chlorophyll content or the reduction of phyll, and this is where different views are some-
leaves to scale-like structures, or both. times entertained. In the majority of such plants,
Numerous mistletoes unquestionably have a no accurate measurements have been made, and
yellowish or brownish coloration. This is often we rely only on observational data. The reliability
the case in squamate plants; however, there are of casual observations becomes more difficult
numerous other examples in Viscaceae where where other pigments mask the chlorophyll.
such species are bright green, and the same can Some students in the past have even taken the
be said for certain Santalaceae. Especially in those position that where the leaves of a parasite are
squamate, green species where internodes have reduced to scales, we must speak of holoparasites
become greatly flattened (e.g., Phthirusa hutchi- even if the stems are bright green. Such a mor-
sonii, and certain species of Korthalsella, Phora- phological definition of holoparasitism can
dendron, and Exocarpos), there can be no doubt scarcely be maintained, especially in view of the
about a significant level of photosynthesis in the numerous Viscaceae and species of Exocarpos
parasite. In mistletoes and others that are not with greatly flattened, bright green internodes,
bright green, photosynthetic pigments may be strikingly so in some Hawaiian Korthalsella. In
masked by other pigments, as probably in some Santalaceae, genera such as Phacellaria and other
dark-colored or reddish-colored Mexican taxa in Australia and the Pacific Islands are in the
Arceuthobium. The curious leafless Tristerix same category. Phacellaria was called “more or
aphyllus of Chile has stems that tend to be bright less holoparasitic” by Stauffer (1969) for such
red, but both chlorophyll a and b are present morphological reasons. On a physiological basis,
(Follmann 1963). Their low level of presence, Glatzel (1987) has defined holoparasites as having
nevertheless, has resulted in the plants being access to phloem sap as well as xylem sap, or
referred to as holoparasites (Kraus et al. 1995). being partially or fully dependent on the host’s
The same controversy is to be found in the litera- photosynthates. This leads him to consider Vis-
ture of Cuscuta (Convolvulaceae), which has cum capitellatum “at least partially a phloem par-
often been called a holoparasite because of low asite” and several Arceuthobium species as “quite
levels of chlorophyll. I am taking the position that holoparasitic”. The notions of “phloem parasit-
holoparasitism refers to the total absence of chlo- ism” and “holoparasitism”, however, are separate
rophyll, irrespective of leaf morphology; from concepts. An entire gradient exists in parasitic
that perspective, the phenomenon is not known plants, generally from bright green, foliaceous
in Santalales. Leaf reduction by itself surely is no plants to true holoparasites. Under the circum-
indication of greater dependence on the host stances, I feel that parasites with any chlorophyll
plant. In Arceuthobium, it is possible that the need to be called semiparasites, as a clear demar-
evolutionary retention of chlorophyll is geneti- cation can otherwise not be drawn. If this line of
cally linked to the significant functional use of argument is followed, all parasites in Santalales
the pigment in the endosperm during seedling are semiparasites.
germination. Whether any of the terrestrial Santalalean
parasites can sustain a non-parasitic existence
Semi- vs. Holoparasitism. The question of the for any length of time has not been sufficiently
degree of photosynthetic activity of parasites has explored. It seems certain that the seedlings of
been a controversial one in parasitic angiosperms root parasites among the mistletoes have a much
more extended independent life expectancy than Barber, C.A. 1908. Studies in root-parasitism. 4. The haus-
arboreal mistletoes; Nuytsia floribunda for at torium of Cansjera rheedii. Mem. Dept. Agric. India,
Bot. Ser. 2(5): 1–36.
least a year (Main 1947). Years ago, I was able to Barlow, B.A. 1971. Loranthaceae. Flora of New South
maintain Gaiadendron punctatum alive and vig- Wales, Fam. No, 58: 1–35.
orous for nearly a year, after which an accident Barlow, B.A., Wiens, D. 1977. Host-parasite resemblance
terminated the effort. Thesium humile is able to in Australian mistletoes: the case for cryptic mim-
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Chemosystematics
By K. Kubitzki. The writer is most grateful to Dr. K. Aitzetm€
uller for his interesting and helpful
comments on the section about acetylenic fatty acids.
The wealth of isolated data on the chemosyste- most of their low-molecular phenolic constitu-
matics of Santalales has been compiled and eval- ents, biogenic amines, protoalkaloids and methy-
uated in the monumental work of Hegnauer lated cyclitols.
(1966–1990), upon which the following overview In the following, the various groups of sub-
largely is based. References given by Hegnauer stances known from Santalales are presented (see
are not repeated here, with the exception of some Table 4), followed by comments on their possible
important papers referred to in the following systematic significance.
discussion and of those which appeared after Among the carbohydrates, the storage of
Hegnauer’s treatments. considerable amounts of myo-inositol and chiro-
Since the members of the Santalales are inositol both in the Loranthaceae and Viscaceae is
mostly hemiparasites, the question arises how remarkable, and these are not taken up from the
far chemical compounds isolated from them host (Plouvier 1953; Hegnauer 1966). From Vis-
may be derived with the uptake from the host cum and Arceuthobium, methylated cyclitols such
plant xylem and possibly phloem, rather than as pinitol and quebrachitol are known which
being genuine products of the parasite itself. seem to be restricted to Viscaceae.
Indeed, it has been demonstrated that natural Carbohydrates are also most important com-
products can pass from the host into the parasite, pounds in the adhesive tissue of the mistletoe
such as cardenolides from Nerium, tropane alka- fruits, which allows the single seed to adhere to
loids from Duboisia, terpenoid hydroxylactones a host branch during germination and withstand
from Coriaria (Okuda et al. 1987), and also vari- the counterforce upon the intrusion of the
ous carbohydrates such as mannitol and querci- absorptive organ of the germinating parasite
tol; also, the leaves of mistletoes growing on into the host tissue. The viscous layer in fruits
coffee and cacao were found to contain almost of Viscum, called viscin, according to Mangenot
as much alkaloids as their host. Hegnauer (1990) et al. (1948) consists of cellulosic filaments
reported that Osyris obviously takes up alkaloids embedded in mucilage which, upon hydrolysis,
from legumes growing in the surroundings, and yields glucose, galactose, arabinose and uronic
in Thesium compounds known from its host, acids. In the two viscaceous species Phoraden-
Globularia, could be found to occur. Sorbitol dron californicum and Arceuthobium ameri-
and scyllo-inositol are present in Viscum album canum analysed by Gedalovich et al. (1988) and
only when they are available in the host, whilst Gedalovich-Shedletzki et al. (1989), the viscin
pinitol, quebrachitol and chiro-inositol are genu- mucilage consisted primarily of neutral sugars,
ine metabolites of the parasite itself. Generally, composed mainly of branched xylans and accom-
the broad-based comparative studies of Plouvier panied by branched arabinans and pectinaceous
(1953) on various species of Loranthaceae and rhamnogalacturonans; uronic acid and proteins
some of their host plants in various parts of the were also present. In the viscin mucilage of the
world have shown that mistletoes are largely loranthaceous Passovia pyrifolia, glucose was the
independent from their hosts with respect to most abundant neutral sugar, accompanied by
44
Table 4. Distribution of some systematically significant natural products in the families of Santalales.
myo- acetylenic essential pentacyclic saponins proline, cyanogenic alkaloids tyramine, polypeptides, condensed hydrolyzable flavonols silicified
and fatty acids oils triterpenes hydroxyproline compounds phenyle- glycoproteins tannins tannins leaf cells
chiro- thylamine
inositol
Coulaceae + +
Ximeniaceae + + + + + + +
Aptandraceae + + + +
Olacaceae + + + + + + (+) +
Octoknemaceae + +
Schoepfiaceae +
Misodendraceae +
Chemosystematics
Loranthaceae + ? + + + + + (+) + +
Opiliaceae + + + + + + (+)
Santalaceae + + + + + + + +
Viscaceae + (+) + + + + + (+) + +
Chemosystematics 45
substantial amounts of xylans and arabinans, and the ene-yne system positioned at C-2 through C-4
the protein content was higher than in the two (El-Jaber et al. 2003).
viscacean samples. Santalbic acid, III (=ximenynic acid), appears
Among the triglycerides, acetylenic fatty to be the most widespread acetylenic fatty acid
acids are the systematically most significant com- isolated from Santalales (Aitzetm€ uller 2012); its
pounds of the Santalales; elsewhere in flowering conjugated ene-yne group implies a median level
plants, they are known from the Compositae and of unsaturation. In Santalales, acetylenic fatty
Simaroubaceae, and have isolated occurrences in acids from vegetative tissues such as leaves,
Afzelia and Sterculia and possibly the liverworts. twigs and bark often have a higher degree of
Within the Santalales, they have been recorded unsaturation than those of seed and fruit. This
from all but two monogeneric, chemically little has been demonstrated by Hatt et al. (1959,
studied families (Schoepfiaceae, Misodendra- 1960) who found santalbic acid amounting to
ceae1); for the Santalaceae, Opiliaceae and Olaca- 60 % of the seed oil of Exocarpus cupressiformis,
ceae, records for numerous genera and species whereas in the roots of the same species an ene-
are available, whereas their presence in the diynoic acid (exocarpic acid, V) formed 89 % of
Loranthaceae and Viscaceae would need further the fatty acids. Bu’Lock and Smith (1963) studied
verification.2 Detailed studies have shown that the occurrence of acetylenic fatty acids in different
various representatives of this class of com- organs of a developing seedling and the seed
pounds commonly occur (usually together with of Santalum acuminatum, and confirmed the
non-acetylenic fatty acids) in the seeds, and are replacement of santalbic acid by more highly
accompanied and often replaced in the vegetative unsaturated fatty acids as the seedling germinated
tissues of the leaves, stems and roots by other and grew. An instructive increase of the level of
representatives of acetylenic fatty acids. These unsaturation in the oils of the vegetative tissue
compounds are formed sequentially from oleic compared with the seed oils is obvious from the
acid (I) via stearolic acid (II) by successive dehy- analyses of two South American Heisteria species:
drogenation steps leading to the acquisition of in the seed oil of the south Brazilian H. silvanii,
conjugated triple bonds and double bonds, start- Spitzer et al. (1997) found trans-10-heptadecen-8-
ing usually at C-9 in the direction towards the ynoic acid (pyrulic acid), trans-11-octadecen-
distal part of the chain (see Table 5). The seven- 9-ynoic acid (santalbic acid), and the three
membered methylene chain (in II–VII) is novel compounds cis-7, trans-11-octadecadiene-
retained in many of these acids in the Santalales 9-ynoic acid (heisteric acid), 9,11-octadecadiy-
of the C-18 type, but there are several deviations noic acid and 13-octadecene-9,11-diynoic acid.
reflecting the great diversity among these sub- From a sample of the bark of the Ecuadorian
stances,3 which is achieved mainly through Heisteria acuminata, Kraus et al. (1998) isolated
increasing desaturation (see examples in Table 5) five new acetylenic fatty acids, namely pentadeca-
but also through processes such as chain- 6,8,10-triynoic acid, octadeca-8,10,12-triynoic
shortening by a-oxidation (e.g. IX) and terminal acid, trans-pentadec-10-en-6,8-diynoic acid,
desaturation (VII, IX). Minquartynoic acid (VI) cis-hexadeca-11-en-7,9-diynoic acid, and cis-
abounds with four conjugated triple bonds octadeca-12-en-7,9-diynoic acid.
(Marles et al. 1989), and the most unusual com- A higher level of desaturation in leaves and
pound found in Santalales seems to be the diacid other vegetative tissue would make sense if a
(X) from the herbaceous Nanodea muscosa with biological significance of acetylenic fatty acids
1
A phenylbutanone has been isolated from Misodendron punctulatum (Reyes et al. 1986); otherwise, such compounds seem to
be unknown in Santalales.
2
Spectroscopic evidence for the presence of acetylenic fatty acids in the vegetative tissue of Nuytsia floribunda and Viscum
album was provided by Hatt and co-workers (Hatt et al. 1960), who also communicated negative results for six species of the
loranthaceous Amyema (Hatt et al. 1967), but in the seed oil of Nuytsia and Viscum the presence of acetylenic fatty acids could
not be verified by Aitzetm€uller (2012).
3
The database SOFA (Seed Oil Fatty Acids; http://sofa.mri.bund.de/) registers 71 acetylenic fatty acid structures with their
botanical sources; 34 of them are C-18 acids with the triple bond in position 9.
46 Chemosystematics
Table 5. A selection of acetylenic fatty acids from the Santalales with their presumed precursor (I), showing the increase of
desaturation (II–VII), examples of terminal desaturation (VII, IX), chain-shortening (IX), and the shift of hydroxylation from
C 7 (IX) to C 17 (VII). I Oleic acid; II stearolic acid; III santalbic acid; IV exocarpic acid; V octadeca-13-ene-9,11-diynoic acid
(from Santalum spp. and Nanodea muscosa); VI minquartynoic acid; VII isanic acid (from Ongokea gore); VIII heisteric acid;
IX 7-hydroxypentadeca-8-yn-10,16-ene acid (from Acanthosyris spinescens); X the unusual dicarboxylic octadeca-2-en-4-
ynedioic acid (from Nanodea muscosa).
CH3 [CH2]7 CH ¼ CH [CH2]7 COOH I
CH3 [CH2]7 C C [CH2]7 COOH II
CH3 [CH2]5 CH ¼ CH C C [CH2]7 COOH III
CH3 [CH2]3 CH ¼ CH C C C C [CH2]7 COOH IV
CH3 [CH2]3 CH ¼ CH C C C C [CH2]7 COOH V
CH3 CHOH C C C C C C C C [CH2]7 COOH VI
CH2 ¼ CH [CH2]4 C C C C [CH2]7 COOH VII
CH3 [CH2]5 CH ¼ CH C C CH ¼ CH [CH2]5 COOH VIII
CH2 ¼ CH [CH2]4 CH ¼ CH C C CHOH [CH2]5 COOH IX
HOOC [CH2]12 C C CH ¼ CH COOH X
could be imputed, because these compounds Pentacyclic triterpenoids such as lupeol, betu-
occur in the leaves in much smaller concentration lin, b-amyrin and oleanolic acid are known from
than in the seeds, and leaves are far more “appar- Viscaceae and Loranthaceae, where they co-occur
ent” resources than seeds. However, I do not with alkanes and alkenes as constituents of cutic-
know whether acetylenic fatty acids are feeding ular waxes. In Santalaceae, triterpenoids were
deterrents and/or protect against fungal or found in the twigs of Exocarpus and fruits of
microbial infection, although a toxic and cyto- Santalum album, whereas in Quinchamalium
toxic activity has been demonstrated for these and Thesium oleanolic acid is the aglycone of a
compounds. saponin. Saponins have further been found in
Among the isoprenoids, caoutchuc (rubber), Olacaceae, Ximeniaceae and Opiliaceae; they are
a polyisoprenoid, is found in considerable mostly based on oleanolic acid but occasionally
amounts in the agglutinant produced by the fruits also on hederagenin or lupeol as the aglycone.
of Loranthaceae (but not Viscaceae). The dried Proline or hydroxyproline or both are typi-
fruits of Loranthus europaeus have been widely in cally found in Santalaceae, Loranthaceae and Vis-
use for the manufacture of birdlime (Schiller caceae. Among the Santalum species, the leaves,
1928); they yielded 36 % (d.w.) of rubber accom- fruits and seeds of S. album are rich in free
panied by pectinaceous mucilage and various hydroxyproline, whereas the leaves of S. mur-
sugars. rayanum contain much proline and few hydroxy-
Essential oils are shared by the Santalaceae, proline and the leaves of S. obtusifolium yielded
Olacaceae, Opiliaceae, Aptandraceae, Ximenia- proline, hydroxyproline and glutaminic acid
ceae and Coulaceae. They occur in the heartwood (Hegnauer 1973).
of stems and branches but not in idioblasts. The Cyanogenic glycosides, which release HCN
classical source of sandalwood oil, which is rich and benzaldehyde, have been recorded from var-
in sesquiterpene alcohols, is the heartwood of the ious families (see Table 4). In Olacaceae, they
Indian Santalum album; other species of Santa- occur in the leaves and other tissues of species
lum yield Australian sandalwood oil, and Osyris of Olax and Chaunochiton; Ximenia americana
tenuifolia is the source of a similar East African (Ximeniaceae) is particularly toxic for livestock,
product. The so-called “Brazilian sandalwood oil” possibly due to the interaction of sambunigrin
is derived from the wood and bark of stems and with the high content of tannin. In Loranthaceae
twigs of Minquartia guianensis, Agonandra bra- and Viscaceae, only few species have been found
siliensis, Aptandra tubicina (the oil of the latter to be cyanogenic.
with a smell of Sassafras) and the roots of Dulacia Alkaloids are on record for various families
guianensis, from which the sesquiterpenoid man- (Table 4), but mostly on the basis of screening
icol has been isolated. reactions, as in the Olacaceae where species of
Chemosystematics 47
Anacolosa, Olax and Strombosia gave positive and Rapson (1938) surveyed South African The-
reactions. These records may, however, some- sium species for condensed tannins and glyco-
times lack reliability; the putatively alkaloidal sides of essential oils, and suggested that
muyrapuamin, a much sought aphrodisiac morphological progressions within the genus
isolated from the roots of Ptychopetalum uncina- are correlated with an increasing loss of both
tum and P. olacoides, has been revealed as a kinds of compounds.
mixture of lipophilic esters with lupeol and behe- Sporadically, ellagic (Nuytsia) and gallic acid
nic acid as the main constituents. From fresh (Heisteria, Tetrastylidium, Okoubaka, Taxillus, in
fruits of Heisteria latifolia, used in Venezuela as the latter as a galloyl glucosid of taxifolin) have
a psychostimulant, the tropine alkaloid scopol- been found in hydrolysates. This might indicate
amine has been isolated, and Dulacia guianensis the presence of hydrolysable tannins, an aspect
yielded the hydroxytropolon manicol. In the San- still needing verification.
talaceae, positive alkaloid reactions were found A wide array of flavonoid compounds occurs
for species of Exocarpus, “Henslowia” (Dendro- in Santalales and is particularly well diversified in
trophe or Dendromyza), Osyris, Santalum and Loranthaceae and Viscaceae, where flavonols, fla-
Thesium. In two Thesium species, necine-type vones, dehydroxyflavones, C-glycoflavones and
alkaloids have been characterised and, since chalcones have been found. Among the various
necines and tropines are biogenetically related, flavonols, glycosides based on quercetin and
their occurrence in the Olacaceae and Santalaceae kaempferol and their methyl ethers abound, whilst
underlines the relationship between the two in the viscaceous, nearly holoparasitic Arceutho-
families (Hegnauer 1984). bium glycosides of myricetin and quercetin are
Loranthaceae and Viscaceae share the pro- omnipresent (36 of the 38 known spp. examined;
duction and storage of considerable amounts of Crawford and Hawksworth 1979); in hydrolysates
tyramine and phenylethylamine. of A. oxycedri prodelphinidin was found. It has
The glycoproteins (lectins) of Viscaceae (vis- been suspected that the strange occurrence of
cotoxins and phoratoxins) are toxic to animals; compounds with trihydroxylated B-rings might
viscotoxins can induce hypertrophic and necrotic be due to uptake from the pinaceous and cupres-
reactions in the host of the mistletoe. These com- saceous hosts, which are known to be rich in them.
pounds are formed by 15–16 amino acid moieties The widespread occurrence of silicified cell
and two sugars, glucose and arabinose, and are groups in the mesophyll (but not in the wood)
widely distributed within but restricted to Visca- in many genera of nearly all families of Santalales
ceae (five genera and 21 spp. tested, and viscotox- (except, apparently, Coulaceae, Opiliaceae and
ins found present in the five genera and nine Octoknema) had been mentioned by Solereder
spp.). Since Viscum album is divided into races (1899, 1908) but subsequently was widely ignored
specialized for different host trees such as pine, until being brought into focus through the work
fir, spruce and various broad-leaved tree species, of Hegnauer (from 1969 onwards; see also Baas
reactions induced by lectins may help to find the et al. 1982). The silica deposition in these hemi-
appropriate host. parasites is remarkable, because some of their
Among the phenylpropanoids, tannins are hosts such as conifers lack this substance.
widely distributed within the order; they have Summarizing, it can be said that the nearly
been isolated mainly from the bark of tree species universal occurrence of acetylenic fatty acids,
of Olacaceae, where they have been found in silicified cells in the leaf tissue and condensed
quantities up to 20 % d.w., but are also recorded tannins underpin the systematic homogeneity of
from Santalaceae, Loranthaceae, Octoknemaceae the Santalales. Although many types of acetylenic
and Ximenia. Usually, they are consensed tan- fatty acids have become known by now, their
nins, which upon hydrolysis yield proanthocya- distribution is still incompletely established so
nidin sometimes accompanied by catechin. that it would be premature to use them for classi-
Condensed tannins, which are widely distributed ficatory purposes within the families, as had been
in woody plants, are viewed as “the most useful of attempted by Hopkins et al. (1969), even if some
all plant chemical defences” (Swain 1978). Kock details of their distribution (such as the presence
48 Chemosystematics
of minquartynoic acid and absence of silica depo- Hatt, H.H., Meisters, A., Triffett, A.C.K., Wailes, P.C. 1967.
sition in the leaves in all three genera of Coula- Acetylenic fatty acids from fats of the Olacaceae and
Santalaceae. V. Austr. J. Chem. 20: 2285–2289.
ceae) may appear systematically meaningful. Hegnauer, R. 1966. Chemotaxonomie der Pflanzen Vol. 4:
Loranthaceae and Viscaceae share the com- 429–438, 501 (Loranth.). Basel: Birkhaeuser.
mon possession of various kinds of compounds - Id. 1969. Vol. 5: 227–231 (Olacac.)
but also differ significantly from each other (see - Id. 1973. Vol. 6: 261–271 (Santalac.)
Hegnauer, R. 1984. Phytochemistry and Chemotaxonomy,
Table 5). Thus, the viscous layer in the fruits of pp. 11–13. In: Sleumer, H.O., Olacaceae. Flora Neo-
Loranthus and other genera of Loranthaceae trop. 38. New York: The New York Botanical Garden.
contains significant amounts of rubber, whereas Hegnauer, R. 1989. Chemotaxonomie der Pflanzen Vol. 8:
Viscaceae fruits lack rubber or are poor in it. In 684–689 (Loranth.)
- Id. 1990. Vol. 9: 149, 156–160, 485–486 (Nachtr.)
contrast to Viscaceae, Loranthaceae are usually Hopkins, C.Y., Chisholm, M.J., Cody, W.J. 1969. Fatty acid
rich in condensed tannins and also contain ellagic components of some Santalaceae seed oils. Phyto-
and gallic acid as possible building stones of chemistry 8: 161–165.
Kock, P.C. de, Rapson, W.S. 1938. A correlation between
hydrolyzable tannins, and toxic polypeptides the chemical constituents and morphological struc-
and glycoproteins are widely distributed but ture of certain Thesium species. Nature 142:
restricted to Viscaceae. This phytochemical evi- 1078–1079.
dence may be considered when Loranthaceae and Kraus, C.M., Neszmélyi, A., Holly, S., Wiedemann, B.,
Nenninger, A., Torsell, K.B.G., Bohlin, L., Wagner,
Viscaceae are evaluated as separate lineages. H. 1998. New acetylenes isolated from the bark of
Heisteria acuminata. J. Nat. Prod. 61: 422–427.
Mangenot, G., Rebiffe, J., Roudier, A. 1948. Sur le muci-
References lage du Gui. Compt. Rend. Acad. Sci. Paris 227:
439–441.
Marles, R.J., Farnsworth, N.R., Neil, D.A. 1989. Isolation
Aitzetm€ uller, K. 2012. Santalbic acid in the plant king- of a novel cytotoxic polyacetylene from a traditional
dom. Plant Syst. Evol. 298: 1609–1617. anthelmintic medicinal plant, Minquartia guianen-
Baas, P., Van Oosterhoud, E., Scholtes, C.J.L. 1982. Leaf sis. J. Nat. Prod. 52: 261–266.
anatomy and classification of the Olacaceae, Octo- Okuda, T., Yoshida, T., Chen, X.M., Xie, J.X., Fukushima,
knema, and Erythropalum. Allertonia 3: 155–210. M. 1987. Corianin from Coriaria japonica A. Gray,
Bu’Lock, J.D., Smith, G.N. 1963. Acetylenic fatty acids in and sesquiterpene lactones from Loranthus parasiti-
seeds and seedlings of sweet quandong. Phytochem- cus Merr. used for treatment of schizophrenia. Chem.
istry 2: 289–296. Pharm. Bull. 35: 182–187.
Crawford, D.J., Hawksworth, F.G. 1979. Flavonoid chem- Plouvier, V. 1953. Sur la recherche des itols et des hetero-
istry of Arceuthobium (Viscaceae). Brittonia 31: sides du gui, Viscum album L. (Loranthaceae).
212–216. Compt. Rend. Acad. Sci. Paris 237: 1761–1763.
El-Jaber, N. et al. 2003. Acetylenic acids from the aerial Reyes, A., Muñoz, M., Garcia, H., Cox, C. 1986. Chemistry
parts of Nanodea muscosa. J. Nat. Prod. 66: 722–724. of Myzodendraceae. I. Myzodendrone, a new phenyl-
Gedalovich, E., Kuijt, J. Carpita, N. 1988. Chemical com- butanone of Myzodendron punctulatum. J. Nat.
position of viscin, an adhesive involved in dispersal Prod. 49: 318–320.
of the parasite Phoradendron californicum (Visca- Schiller, F. 1928. Zur Kenntniss der Frucht von Viscum
ceae). Physiol. Mol. Plant Pathol. 32: 61–76. album und Loranthus europaeus und der Gewinnung
Gedalovich-Shedletzky, E., Delmer, D.P., Kuijt, J. 1989. von Vogelleim. Sitz. ber. Akad. Wiss. Wien, Math.-
Chemical composition of viscin mucilage from naturw. Kl. Abt. 1, 137: 243–258.
three mistletoes – a comparison. Ann. Bot. 64: Solereder, H. 1899. Systematische Anatomie der Dicotyle-
249–252. donen (pp. 818–823). Stuttgart: Enke, with Erg€an-
Hatt, H.H., Triffett, A.C.K., Wailes, P.C. 1959. Acetylenic zungsband (1908): 284–285.
fatty acids from fats of Santalaceae and Olacaceae: Spitzer, V., Tomberg, W., Hartmann, R., Aichholz, R.
seed and root oils of Exocarpus cupressiformis Labill. 1997. Analysis of the seed oil of Heisteria silvanii
Austr. J. Chem. 12: 190–195. (Olacaeae) – a rich source of a novel C18 acetylenic
Hatt, H.H., Triffett, A.C.K., Wailes, P.C. 1960. Acetylenic fatty acid. Lipids 32: 1189–1200.
fatty acids from fats of Santalaceae and Olacaceae. Swain, T. 1978. Tannins and lignans, pp. 657–682. In:
IV. The occurrence of octadeca-trans-11, trans 13- Rosenthal, G.A., Janzen, D.H. (eds) Herbivores,
dien-9-ynoic acid in plant lipids. Austr. J. Chem. 13: their interaction with secondary plant metabolites.
488–497. New York: Academic Press.
Santalales in Human Affairs and Conservation
Human Affairs. The economic issues involving tent, sweet fragrance, and are used in rituals of
Santalales are relatively modest except for the several Eastern religions, either as oil or as a soft
two or three ones mentioned below. Many of paste applied to the forehead and upper body, or
the trees in the order are locally prized for as incense. In the late 18th century, the rise of the
their superior wood qualities. This is true for Kamehameha royal dynasty in Hawai’i is credited
Acanthosyris, Coula, Heisteria, Minquartia, Scor- largely to the exploitation of local Santalum spe-
odocarpus, Strombosia, and Strombosiopsis. The cies to accommodate the Chinese market, eventu-
relevant sources of information, however, are ally resulting in the near-extinction of at least one
dated, and the increasing disappearance of tropi- species, S. freycinetianum, which is now classified
cal forests may have rendered some of them no as threatened. In fact, a related species, “S. fernan-
more than a historical fact. In a few cases, fruits dezianum” (Mida salicifolia), was actually driven
are edible (Coula, Ximenia, and even the fruits of to extinction on the Juan Fernandez Islands of
Lysiana casuarinae in Australia are consumed by southern Chile. The wood of S. album, aside
the Nyoongar people according to Watson 2011). from its fragrance and source of oil, is prized for
Young shoots of both Champereia and Melientha its hardness and fine grain, and for the ability to
are used as a vegetable in Thailand (Kubat 1987), retain its fragrance for decades. There are substi-
even though there may be toxic issues. The curi- tutes for S. album, including Ximenia (Sleumer
ous, small tubers of Arjona have also been used as 1984) and several species outside Santalales, but
a minor food source in southern South America none have the outstanding qualities of the true
(Fig. 4). sandalwood. In our day, aside from its religious
In a separate category is Ptychopetalum of uses, sandalwood oil continues to be prized in the
South America, the bark and roots of which are manufacture of soaps and cosmetics.
used to prepare an aphrodisiac called “Muira- The most common European mistletoe, Vis-
puama” that also has some local medicinal uses, cum album, may justifiably be called the most
and continues to be marketed today. The wood of famous plant alive. Its fame goes back to the
Minquartia yields a black dye employed in the ancient Edda sagas of Iceland in the early 13th
working of wool and other textiles. century, where mistletoe plays a central role
Beyond such minor and often exclusively local (Kuijt 1969). There is evidence, however, that
usages, there are some issues in Santalales that are the main motif is much older, and that it origi-
of genuine economic importance. The sandal- nated much further south (conceivably even in
wood tree, Santalum album, a native of southern Asia Minor), for V. album has probably never
India but cultivated for centuries throughout been native to Iceland. Medieval European
much of tropical Asia, has served since times records show that the species was used medici-
immemorial to extract essential oils from its nally for a variety of ills and to ward off evil, and
wood and roots. The oils have a famous, persis- such uses may well be the precursors of the
50 Santalales in Human Affairs and Conservation
The Austrian mystic and educator Rudolf

Steiner (1861–1925) early in his life conceived of
the idea that V. album contained substances that
could be used to control cancer. He eventually
elaborated this central notion to indicate that the
parasite, when growing on different hosts, had
such effects on different types of cancer. His
ideas have led to the manufacture of several
extracts that continue to be available commer-
cially in Europe and South Africa, Iscador being
the most important. The efficacy of such treat-
ments remains very controversial, however. A
modern analysis of relevant publications finds
that “evidence of clinical benefit from human
studies remains weak and inconclusive”, and
that there is “limited evidence that mistletoe pro-
ducts may offer some therapeutic advantage”
(Kaegi 1998; Ernst et al. 2003).
There are isolated instances of Santales being
used medicinally, usually not yet confirmed by
modern medical science. Viscum articulatum in
Australia has served for the treatment of stomach
complaints and high blood pressure, and Diplatia
grandibracteata is widely used as a poultice to
treat sores (Watson 2011). A variety of similar
uses is listed in my monographs of Phoraden-
dron, Psittacanthus, and Dendropemon (Kuijt
Fig. 4. Subterranean parts of Arjona tuberosa with roots 2003, 2009, 2011). In southern Chile, Quinchama-
(r) and tuber-producing rhizomes originating from the lium is being gathered and offered for sale in local
base of new inflorescences extending from old tubers.
(Kuijt 1969, drawn by author) markets as a folk medicine for unknown maladies
(pers. observ.).
A very different economic issue is the damage
well-known and continuing Christmas lore that to forest trees through the parasitism of dwarf
shows no evidence of abating in our time. Eur- mistletoe species of the genus Areuthobium, par-
opeans migrating to other parts of the world ticularly in western North America. In many
carried such traditions with them, often making areas, both in Canada and the United States,
use of local mistletoes. Particularly in the United dwarf mistletoes constitute the most damaging
States, where some native species of Phoraden- pathogens of coniferous forests. Hawksworth
dron resemble V. album and are common in and Wiens (1996) speak of losses of several bil-
many areas, the cult of mistletoe survives and lions of dollars annually. The effects of Arceutho-
seasonal trade of the plant continues notwith- bium parasitism are numerous. There is, first of
standing its plastic surrogates. Less known is the all, growth retardation of the host. Secondly, par-
fact that the viscin of fruits of V. album has often asitism by dwarf mistletoes is associated with
been employed to capture small birds, a practice various types of growth abnormalities, especially
that was known to the ancients in the Mediterra- (in some host-parasite combinations) the forma-
nean and also has been carried to some foreign tion of large “witches’ brooms” that render trees
localities. The species has inspired many artists valueless economically. Fungi and insects are
and craftsmen (Becker and Schmoll 1986). often attracted to parasitized trees. Species of
References 51
Abies, Larix, Picea, Tsuga, and especially many References

species of Pinus are locally affected. No effective
silvicultural or chemical control measures have Becker, H., Schmoll, H. 1986. Mistel. Arzneipflanze,
been devised except, of course, clear-cutting. Brauchtum, Kunstmotiv im Jugendstil. Stuttgart:
Other mistletoes are also important tree patho- Wissensch. Verlagsgesellschaft.
Ernst, E., Schmidt, K., Steuer-Vogt, M.K. 2003. Mistletoe
gens in the tropics, such as those on teak (Tectona for cancer? A systematic review of randomized clini-
grandis) in Asia; frequently, poor cultivation cal trials. Int. J. Cancer 107: 262–267.
practices allow plantations of cacao and other Hawksworth, F.G., Wiens, D. 1996. Dwarf mistletoes: biol-
commercial trees to be seriously infested. ogy, pathology, and systematics. U.S.D.A., For. Serv.,
Agric. Handb. 709, Washington, D.C.
Kaegi, E. 1998. Unconventional therapies for cancer: 3.
Conservation. In the last two decades, there has Iscador. Can. Med. Ass. J. 158: 1157–1159.
been a growing awareness of the ecological sig- Kubat, R. 1987. Report of the first investigations of para-
nificance of mistletoes in ecology. Dense mistle- sitism in Opiliaceae (Santalales). Proc. 4th Interna-
tional Symposium on Parasitic Plants, pp. 489–492.
toe bushes as well as Arceuthobium brooms often Marburg, Germany.
provide nesting opportunities for birds, and both Kuijt, J. 1969. The biology of parasitic flowering plants.
fruits and nectar of mistletoes elsewhere can be Berkeley and Los Angeles: Univ. Calif. Press.
important avian food sources. Nectar Kuijt, J. 2003. Monograph of Phoradendron (Viscaceae).
Syst. Bot. Monogr. 66: 1–643.
feeds insects that are significant pollinators Kuijt, J. 2009. Monograph of Psittacanthus (Lorantha-
generally. In western Canada, Arceuthobium ceae). Syst. Bot. Monogr. 86: 1–361, Frontispiece.
americanum flowers before any other local plants Kuijt, J. 2011. Monograph of Dendropemon (Lorantha-
do. The awareness of the ecological status of ceae). Syst. Bot. Monogr. 92: 1–110.
Sleumer, H. 1984. Olacaceae. Flora Neotropica 38: 1–159.
mistletoes in New Zealand has led to attempts to New York: Organiz. For Fl. Neotrop.
protect them against the introduced Australian Watson, D.M. 2011. Mistletoes of Southern Australia.
opossums. Collingwood, Australia: CSIRO Publishing.
Family Classification
Summary of Changes. The most significant six tribes. Nickrent et al. (2010) distributed these
changes in which the family classification genera over six families (Aptandraceae, Coula-
adopted in this treatment differs from the one ceae, Olacaceae s.s., Strombosiaceae, Schoepfia-
suggested by Nickrent et al. (2010) and Der and ceae, and Ximeniaceae), none of which was
Nickrent (2008) (see Table 1, p. 49) are as follows: further subdivided; these families are here
retained except that Strombosiaceae are placed
1. Erythropalaceae. The systematic affinities of Ery-
in synonymy under Olacaceae. Brachynema,
thropalum have yet to be resolved. Nickrent et al.
here placed in Olacaceae, was excluded in the
(2010) maintained it in Santalales, uniting it with
molecular studies by Malécot et al. (2004) and
Heisteria and Maburea in Erythropalaceae. While
Nickrent et al. (2010) (see the discussion under
a phylogenetic relationship between Heisteria
that genus).
and Maburea in my opinion is quite arguable,
8. Worcesterianthus Merrill, Philip. J. Sci. Bot. 9:
their affinity to Erythropalum strains credulity.
288 (1914). The genus was tentatively placed in
It is essentially impossible to propose a coherent
Olacaceae tribe Anacoloseae by Sleumer (1935),
family description for these three genera. I follow
but he doubted its correct placement in Olacaceae
Sleumer (1935) in removing Erythropalaceae
partly because its fruit has two compartments
from Santalales and placing Heisteria in Olaca-
each with a single seed, which would be unique
ceae, and I place Maburea in that same family,
in Santalales. The genus is excluded from the
where it was originally described by Maas et al.
present treatment, and may belong to Epacrida-
(1992).
ceae or Icacinaceae.
2. Santalaceae in the present treatment are taken
to include Amphorogynaceae, Cervantesiaceae
Santalalean Families as Presently Accepted:
(including Pilgerina and Staufferia), Comandra-
ceae, Nanodeaceae, and Thesiaceae. Aptandraceae
3. Eremolepidaceae are maintained as a separate Aptandra, Chaunochiton, Harmandia, Honduro-
family. dendron, Ongokea, Phanerodiscus
4. I move Arjona and Quinchamalium from Coulaceae
Schoepfiaceae and place them in Santalaceae s.l., Coula, Minquartia, Ochanostachys
where they have been in the past. Eremolepidaceae
5. Anthobolus is moved from Opiliaceae, rejoining Antidaphne, Eubrachion, Lepidoceras
other Santalaceae. Loranthaceae (numerous genera)
6. Anacolosa and Cathedra are moved from Aptan- Misodendraceae
draceae and restored to Olacaceae. Misodendrum
7. Olacaceae were treated by Sleumer (1935) as Octoknemaceae
consisting of 23 genera in three subfamilies and Octoknema
54 Family Classification
Olacaceae ovule reduction, we may perceive convincing,

Anacolosa, Brachynema, Cathedra, Diogoa, Dulacia, individual trends: the evolution of the ovarian
Engomegoma, Heisteria, Maburea, Olax, Ptychope- papilla in Exocarpos can be traced to the more
talum, Scorodocarpus, Strombosia, Strombosiopsis, common pendulous ovules in other Santalaceae,
Tetrastylidium and the total disappearance of the ovarian papilla
Opiliaceae and even the ovarian cavity in some Viscum spe-
Agonandra, Cansjera, Champereia, Gjellerupia, cies form a more advanced condition than that of
Lepionurus, Melientha, Opilia, Pentarhopalopilia, other species. But we have no indication what-
Rhopalopilia, Urobotrya ever in these two situations that the more
Santalaceae advanced condition is associated with an
Acanthosyris, Amphorogyne, Anthobolus, Arjona, increased level of parasitism, however this is con-
Buckleya, Cervantesia, Choretrum, Colpoon, Coman- ceived. The logical connection between the two
dra, Daenikera, Dendromyza, Dendrotrophe, Dufre- trends escapes us. In consequence, an alignment
noya, Exocarpos, Geocaulon, Jodina, Kunkeliella, of families according to increasing parasitism,
Leptomeria, Mida, Myoschilos, Nanodea, Nestronia, however appealing a prospect, must remain an
Okoubaka, Omphacomeria, Osyridicarpos, Osyris, illusionary effort.
Phacellaria, Pilgerina, Pyrularia, Quinchamalium,
Rhoiacarpos, Santalum, Scleropyrum, Spirogardnera, A Note on the Term “Mistletoe”. Before proceed-
Staufferia, Thesidium, Thesium ing to a consideration of individual Santalalean
Schoepfiaceae families, it is useful to focus on the term “mistle-
Schoepfia toe” and its other European equivalents. Prior to
Viscaceae the extensive exploration of non-European areas
Arceuthobium, Dendrophthora, Ginalloa, Korthal- or even into the 20th century, the concept was
sella, Notothixos, Phoradendron, Viscum scarcely controversial because the known mistle-
Ximeniaceae toes could be defined as flowering plants parasitic
Curupira, Douradoa, Malania, Ximenia on branches of shrubs or trees and were placed in
a single family, Loranthaceae. The discovery of
Sequence of Families. There have been repeated genera such as Nuytsia and Phacellaria, however,
suggestions in the Santalalean literature, perhaps produced problems quite distinct from the even-
originating in Van Tieghem’s writings, of a possi- tual taxonomic recognition of Viscaceae as a sep-
ble evolutionary progression towards increasing arate family from Loranthaceae. Nuytsia clearly
parasitism as associated with ovule reduction and belongs in Loranthaceae, but is exclusively a root
other embryological events. It must be pointed parasite; Phacellaria, in contrast, is an obligate
out that it is not clear what is meant by “increas- parasite on the branches of other plants, but is a
ing parasitism”. Physiologically, it would seem to member of Santalaceae. Are these genera never-
entail an increased dependency on the host, prob- theless to be called mistletoes? The concept “mis-
ably a presumed switch to the host phloem as a tletoe” thus has lost some of its purely taxonomic
(not necessarily direct) source of targeted materi- framework to become somewhat more of an eco-
als combined with a decreased photosynthetic logical concept, a matter of life style, but always
capacity of the parasite. There have been individ- allowing for inclusion of root-parasitic, terrestrial
ual demonstrations of the latter differences, as in or semi-terrestrial Loranthaceae. We have come
a comparison between a leafy Phoradendron and to realize that the branch-parasitic mistletoe
squamate Arceuthobium (Hull and Leonard habit has evolved multiple times.
1964a, 1964b), placing the latter at a more All mistletoes are parasitic (which here is
advanced level. It is not clear how such informa- accepted to mean that they penetrate host tissue
tion can support generalizations in the order. by means of specialized haustoria active in the
With regard to the curious developments in absorption of nutrients and/or water), but there
the ovular region, we are faced with parallel pro- was some early uncertainty of this fact in the
blems. The numerous bizarre embryological root-parasitic members like Gaiadendron and
developments in various families and genera pro- especially in Nuytsia, where the question was
vide no comparative material. In the matter of eventually clarified by Herbert (1919).
References 55
References adendron). II. The photosynthetic capacity of mistle-

toe. Plant Physiol. 39: 1008–1017.
Maas, P.J.M., Baas, P., Boesewinkel, F.D., Hiepko, P.,
Der, J., Nickrent, D.L. 2008. A molecular phylogeny of Lobreau-Callen, D., Van den Oever, L., Ter Welle,
Santalaceae (Santalales). Syst. Bot. 33: 107–116. B.J.H. 1992. The identity of “Unknown Z”: Maburea
Herbert, D.A. 1918–1919. The West Australian Christmas Maas, a new genus of Olacaceae in Guyana. Bot.
Tree, Nuytsia floribunda – (The Christmas Tree) – its Jahrb. Syst. 114: 275–291.
structure and parasitism. J. Roy. Soc. W. Austr. 5: Malécot, V., Nickrent, D.L., Baas, P., Van den Oever, L.,
72–88. Lobreau-Callen, D. 2004. A morphological cladistic
Hull, R.J., Leonard, O.A. 1964a. Physiological aspects of analysis of Olacaceae. Syst. Bot. 29: 569–586.
parasitism in mistletoes (Arceuthobium and Phora- Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
dendron). I. The carbohydrate nutrition of mistletoe. 2010. A revised classification of Santalales. Taxon
Plant Physiol. 39: 996–1007. 59: 538–558.
Hull, R.J., Leonard, O.A. 1964b. Physiological aspects Sleumer, H. 1935. Olacaceae. In: Engler, A., Prantl, K., Die
of parasitism in mistletoes (Arceuthobium and Phor- nat. Pflanzenfam., 2nd edn, 16b: 5–32.
Key to the Families of Santalales
1. Terrestrial trees, shrubs, or herbs, whether root- 8. Phyllotaxy alternate Santalaceae (Daenikera,
parasitic or not 9 Phacellaria)
– Parasites on the branches or trunks of woody – Phyllotaxy paired Viscaceae (Viscum, Ginalloa,
plants (in the case of Gaiadendron, parasitic on Notothixos)
epiphytes) 2 9. Flowers with erect, fleshy, evascular structures
2. Ovary and fruit minute, with 3 conspicuous, lon- alternating adaxially with the distinct stamens
gitudinal grooves; fruit with 3 long, external, and rarely forming a connate short tube
feather-like setae; staminate flower apetalous, Opiliaceae
reduced to 2 or 3 monothecal stamens; Andean – Flowers with or without disk, this not consisting
forests of South America, mostly from 36 S of erect, fleshy structures; stamens often epipeta-
southwards Misodendraceae lous, or synandrous 10
– Ovary and fruit lacking longitudinal grooves; 10. Stamens united in a synandrium, or anthers at
fruit without external setae; staminate flower the tip of filaments, in either case opening in
with petals (some staminate Antidaphne with- valvate fashion (see Phanerodiscus)
out); subtropical and tropical areas worldwide, Aptandraceae
and some temperate regions 3 – Stamens not united in a synandrium; when basi-
3. Calyculus present (at least in pistillate flowers if fixed, anthers not valvately dehiscent 11
separate) Loranthaceae 11. Ovary inferior, subtended by bracteal cup
– Calyculus absent 4 formed from one bract and two prophyllar brac-
4. Squamate plants parasitic on N Hemisphere teoles; flowers distylous 12
conifers Viscaceae (Arceuthobium) – Ovary inferior or superior, bracteal cup absent
– Parasitic mostly on non-conifers; if on conifers, (but calyculus sometimes enlarging in fruit);
not squamate or not N Hemisphere 5 flowers not distylous except Dulacia and Ptycho-
5. New World 6 petalum (Olacaceae) 13
– Old World 8 12. Trees or shrubs; bracteal cup clasping only the
6. Phyllotaxy alternate base of the fruit; post-staminal hair tuft lacking;
Eremolepidaceae (Antidaphne, Eubrachion) pantropical Schoepfiaceae
– Phyllotaxy decussate 7 – Low herbaceous plants; fruit completely
7. Flowers sessile, placed along inflorescence enclosed by sclerified bracteal cup; post-staminal
internodes Viscaceae (Phoradendron and Den- hair tuft present; C Peru and N Argentina south-
drophthora) wards Santalaceae (Quinchamalium)
– Flowers pedicellate, either racemic (staminate) or 13. Trees or shrubs, the latter with paired leaves;
individually in leaf axils (pistillate) flowers subtended by both bracts and prophyllar
Eremolepidaceae (Lepidoceras)
58 Key to the Families of Santalales
bracteoles; not in S Africa Loranthaceae (Atkin- 15. Leaves with resin ducts and laticifers; calyculus
sona, Nuytsia, Gaiadendron) small, not accrescent; stamens in 1–3 whorls,
– Prophyllar bracteoles absent unless (Santalaceae: distinct except in Minquartia; ovary broadly
Thesidium, some Thesium) plants herbaceous conical Coulaceae
and leaves alternate (but see Strombosiopsis, – Leaves without resin canals or laticifers;
W Africa) 14 calyculus absent (in some Olacaceae and Strom-
14. Plants dioecious; young growth with dense, stel- bosiaceae) or accrescent; stamens epipetalous or
late hairs; stigma with 3–5 spreading, fissured distinct; ovary not broadly conical 16
or dentate lobes; endosperm deeply furrowed 16. Calyculus absent (but see Buckleya); post-
Octoknemaceae staminal hair tuft mostly present; all genera
– All flowers bisexual (Buckleya and Thesidium parasitic Santalaceae
dioecious; Geocaulon with some functionally – Calyculus absent or present (then sometimes
male flowers, Santalaceae); plants glabrous or accrescent in fruit); post-staminal hairs mostly
at least without stellate hairs; stigma simple absent but filaments sometimes hairy; parasitic
or very short-lobed; endosperm not furrowed or not Olacaceae
15
Aptandraceae
Aptandraceae J. Miers in Lindl., Veg. Kingd., ed. 3: 447a (1853).
Chaunochit(on)aceae Tiegh. (1896).
Harmandiaceae Tiegh. (1898).
Trees or large shrubs with simple, petiolate, exsti- and Hondurodendron. They also, in the key to
pulate leaves, phyllotaxy alternate. Inflorescence families, refer to the family as being parasitic,
a raceme or panicle or crowded cluster, usually but this fact has not been demonstrated for any
axillary. Flowers mostly bisexual (unisexual in of the component genera, even in the relevant
Harmandia and Hondurodendron). Petals 4–8, work of Teo (1997).
calyx/calyculus present, often greatly enlarging Phanerodiscus, when described by Cavaco
and enclosing most or all of the fruit (persistent (1954) and later reviewed by Malécot et al.
but not accrescent in Phanerodiscus, where the (2003), was at that time placed in Olacaceae, but
fruit envelope is of different origin), its apex was subsequently reassigned to Aptandraceae by
expanding in trumpet-like fashion beyond the Nickrent et al. (2010).
fruit in Hondurodendron. Stamens epipetalous The major diagnostic criterion of Aptandraceae
or filaments connate into a synandrial tube, dis- appears to lie in its unique androecial modifica-
tinct in Hondurodendron; anthers small, termi- tions. In several genera (Aptandra, Chaunochiton,
nally placed on the filaments, opening in valvate Hondurodendron, and Harmandia), the anthers
fashion in most genera; in Phanerodiscus with dehisce by means of valvate flaps rather than longi-
6–8 pores placed in U-shaped pattern on anther tudinal slits; in Aptandra, Harmandia, and Ongo-
margins. Pollen of Hondurodendron is isopolar, kea, the filaments are connate to form a synandrial
shallowly tubercular, oblate in equatorial view, tube. Phanerodiscus, first placed in Olacaceae by
triangular, tricolporate with broad colpi nearly Malécot et al. (2003, 2004), has a curious, U-shaped
meeting at the poles; Chaunochiton has a pollen configuration of 6–8 pores on the margin of the
sculpturing that is unique in Santalales (see anther. Neither Anacolosa nor Cathedra, both
below). Ovules ategmic or unitegmic. Fruit a placed in Aptandraceae by Nickrent et al. (2010),
one-seeded drupe with stony exocarp, endosperm share such fundamental features, having a more
copious; cotyledons 2. regular anther structure; for this reason, a system-
A family presently comprising six genera, all atic placement in Olacaceae remains more appro-
of which were until recently included in Olaca- priate. Aptandraceae thus emerges as a family of
ceae except Hondurodendron, as published by considerable integrity, characterized by its curious
Ulloa et al. (2010) contemporaneously with anthers that are placed at the tip of the filaments
Nickrent et al.’s (2010) reorganization of the and dehisce by means of valves rather than fissures,
order Santalales. The latter authors refer to two by (some genera only) synandria, and by an accres-
clades in Aptandraceae, one containing Anaco- cent calyx growing beyond the fruit or tightly
losa, Cathedra, and Phanerodiscus, the other one enclosing it at maturity. Phanerodiscus, however,
Aptandra, Chaunochiton, Harmandia, Ongokea, remains a genus of problematic assignment.
60 Aptandraceae
POLLEN. The pollen of Aptandra is heteropolar and

tetracolpate, with ectoapertures in the shape of a
small groove or more or less rectangular (Bonne-
ville et al. 1982).
The fossil pollen known as Anacolosidites
Cookson and Pike, first placed in Olacaceae, is
probably assignable to Phanerodiscus of the pres-
ent family (Malécot et al. 2004). It is present in the
Maestrichtian (72 Ma) in both northern and
southern hemispheres (Muller 1981; Askin 1989;
Krutzsch 1989), and in the Eocene (53 Ma) of
Africa and India (Kuyl et al. 1955; Thanikaimoni
et al. 1984; Lucas 1994), when members of this
tribe apparently entered Madagascar.
The pollen of Chaunochiton has extraordinary
sculpture features, its surface being sharply divided
into psilate, circular equatorial areas and fused col-
pal margins that are strikingly raised in densely
lobed fashion (Feuer 1977). It is a pollen structure
that is unique in the order and possibly beyond.
KEY TO THE GENERA OF APTANDRACEAE
1. Stamens united in a tube surrounding the style 2

– Stamens not united 4
2. Flowers unisexual; petals 4 (staminate) or 6–8 (pistil-
late) 3. Harmandia
– Flowers bisexual; petals 4 or 5 3
3. Petals 4, ovules 2 1. Aptandra
Fig. 5 Aptandraceae. Aptandra tubicina. A Flowering
– Petals 5, ovules 3 5. Ongokea branchlet. B Flower bud. C Open flower. D Stamen tube
4. Dioecious, petals 4; Honduras 4. Hondurodendron at early anthesis. E Same, in a later stage with dehiscent
– Flowers bisexual, petals 5 or 6; not in Central America anthers. F Flower longitudinally sectioned. G Ovary and
(Chaunochiton reported for Costa Rica) 5 style, longitudinally sectioned. H Immature fruit with
fruit-calyx. I Same, cut open. (Sleumer 1984)
5. Petals linear; fruiting calyx funnel-shaped, not cover-
ing the fruit; stamens long, filaments; South America
and Costa Rica 2. Chaunochiton
– Petals not linear; the fruit enclosed by several distinct
lobes; stamens short, not hair-like; Madagascar bisexual, with very small, 4-toothed, calyculus
6. Phanerodiscus becoming large and funnel-shaped or urceolate
around the fruit at maturity. Petals 4, fleshy, linear
to tongue-shaped, recurving at anthesis. Glandular
GENERA OF APTANDRACEAE disk with 4 fleshy lobes between the petals and
stamens. Stamens 4, united into a cylindrical
1. Aptandra Miers Fig. 5 synandrium, the anthers forming a ring, the
locules dehiscing by a flap that bends downwards.
Aptandra Miers, Ann. Magaz. Nat. Hist. II, 7: 201 (1851). Ovary ovoid to conical, 2-chambered below with
2 pendent ovules; stigma with clavate tip. Fruit a
Trees with thin, elongate-elliptical alternate drupe with hard endocarp, 1-seeded.
leaves with acute apices. Inflorescence terminal Four spp., three in tropical South America
or axillary, simple or branched panicles. Flowers and one in West Africa.
GENERA OF APTANDRACEAE 61
nearly spherical, at the tip of the filament, and

opening with 2 or more flaps. Ovary superior, 5-
ribbed lengthwise, elongate, 2-loculate basally, sim-
ple above, with 1 ovule suspended in each locule;
style at least as long as the stamens, stigma capitate,
5-lobed. Fruit ca. 5-sided, spherical, longitudinally
5–10-grooved or warty, with one seed, fruit wall
thin; fruiting calyx very large, profusely veined.
Three spp., one in Brazil, the others from
NW South America (Brazil, Guianas, Venezuela,
Colombia), one species reportedly also in Costa
Rica.
3. Harmandia Pierre ex Baillon
Harmandia Pierre ex Baillon, Bull. Soc. Linn. Paris 2: 770

(1889).
Trees with distichous, lanceolate leaves.

Inflorescences axillary panicles. Flowers pedicel-
late, unisexual, calyx small, dish-shaped, with 4
short teeth, enlarging in fruit and enclosing it.
Petals 4 (staminate) or 6–8 (pistillate), more or
less campanulate. Glandular disk ring-shaped,
evanescent. Stamens 4, united in a synangium,
the connectives of the anthers fusing and nearly
closing the terminal pore. Ovary pyramidal,
ovules 2, pendent from a short funiculus, stigmas
3, sessile. Fruit a drupe, connate with the calyx
below, 1-seeded.
One sp., H. mekongensis Pierre, continental
SE Asia.
4. Hondurodendron Ulloa, Nickrent, Whitefoord &
Fig. 6 Aptandraceae. Chaunochiton angustifolium. Kelly
A Flowering branchlet. B Flower. C Petal inside with stamen.
D Fruit with expanded flattened calyx. (Sleumer 1984)
Hondurodendron Ulloa, Nickrent, Whitefoord, and Kelly,
Ann. Missouri Bot. Gard. 97: 457–467 (2010).
2. Chaunochiton Benth. Fig. 6 Dioecious trees to 12 m high, young shoots

densely covered by short reddish brown hairs.
Chaunochiton Benth. in Benth. & Hook. f., Gen. Plant. 1: Leaves distichous, petiolate, elliptic to lanceolate,
996 (1867). apex acute and more or less acute basally, shiny
above, whitish-green below, glabrescent, forming
Small to moderate trees. Leaves alternate, pin- flattened sprays. Inflorescences axillary. Male
nately veined, petiolate, glabrous. Inflorescence an inflorescence with to ca. 20 flowers in few-flowered
axillary, short-pedunculate, corymb-like panicle cymose units, bracts linear, densely reddish
with few to many flowers. Flowers fragrant, with tomentose; flowers externally tomentose; calyculus
small, cupulate, 5-dentate calyx much enlarged in cup-shaped, very short, the rim minutely denticu-
fruit. Petals 5, distinct, linear-elongate, most of the late; petals 4. Stamens as many as, and opposite
adaxial surface pilose. Glandular disk small. the petals; filaments distinct, erect, bearing termi-
Stamens 5, epipetalous, opposite the petals and nal, basifixed, 3-lobed anthers dehiscent by as
nearly as long, filaments thread-like; anthers small, many longitudinal valves; pollen isopolar,
62 Aptandraceae
triangular in polar view, tricolporate, the colpi

nearly meeting at the poles; glandular disk with
lobes alternating with the stamens. Female inflor-
escences shortly spicate, flowers to 4, each sub-
tended by 1.5 mm long bract and 2 small
bracteoles, densely reddish tomentose; flowers
with cup-shaped calyculus with entire rim, petals
4 or 5(6), deltoid; ovary superior, broadly ovoid,
densely pubescent, 2-chambered basally but
united above, ovules 2, pendent from a distinct
central placental stalk; style short, stigma thick,
round. Fruit a shallowly furrowed drupe,
completely enveloped by the accrescent, coria-
ceous calyx extending beyond the fruit in cup-
shaped, deeply fissured fashion; exocarp thin.
A single sp., H. urceolatum Ulloa, Nickr.,
Whitef. & Kelly; known only from NW Honduras. Fig. 7 Aptandraceae. Ongokea gore. A Flowering branch.
5. Ongokea Pierre Fig. 7 B Part of inflorescence with applanate axes. C Part of
inflorescence with young buds. D Further developed
bud. E Open flower. F Fruiting branchlet with fruits
Ongokea Pierre, Bull. Soc. Linn. Paris 2: 1313 (1897). enclosed by enlarged calyx. G Fruit and seed, longitudinal
section. (Engler 1915)
Trees resembling Aptandra. Flowers bisexual.
Petals 5, distinct, tongue-shaped, recurving in
anthesis; calyx very small, dish-shaped, with 5 shorter (glandular?) hairs below; filaments short,
short teeth. Stamens 5, united in a synangium as anthers basifixed, biloculate, with 6–8 pores in
in Aptandra, the anthers dehiscing with valvate U-shaped pattern on the anther’s margin. Ovary
flaps; 5 thick lobes separating synandrium and superior, style stout, hairy in or above the middle,
petals. Ovary ovoid, ovules 3, pendent from the stigma scarcely differentiated. Fruit a drupe sur-
central funiculus. Fruit 1-seeded, at maturity rounded by an accrescent membranous structure,
completely enclosed by the enlarged calyx, eventu- either entire or partially so with several erect
ally splitting into 3 parts; embryo small, dicotylous. lobes exceeding the fruit, this envelope being
One sp., Ongokea gore (Hua) Pierre, western profusely vasculated.
tropical Africa. Three spp., endemic to Madagascar.
Ongokea appears to differ from Aptandra The revision of Phanerodiscus by Malécot et al.
mainly in having 3, rather than 2 ovules, and in (2003) still placed it in Olacaceae, but the genus was
having 5-merous rather than 4-merous flowers. moved to Aptandraceae in Nickrent et al. (2010). Its
The two genera could conceivably be united. familial position remains uncertain, the unique fruit
envelope being of puzzling homology.
6. Phanerodiscus Cavaco
Phanerodiscus Cavaco, Notul. Syst. (Paris) 15: 11 (1954).

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Syst. Evol. 162: 5–61. Teo, S.P. 1997. Root hemi-parasitism in Malayan Olaca-
Kuyl, O.S., Muller, J., Waterbolk, H. 1955. The applica- ceae. Gardens Bull. Singapore 49: 7–13.
tion of palynology to oil geology with reference to Thanikaimoni, G., Caratini, C., Venkatachala, B.S., Ramanu-
western Venezuela. Geol. & Mijnb., n.s. 3: 49–76. jam, C.G., Kar, R.K. 1984. Pollens d’Angiospermes du
Lucas, F.A. 1994. A miospore (pollen and spores) biozo- Tertiaire de l’Inde et leurs relations avec les pollens du
nation model for the late Cretaceous to middle Tertiaire d’Afrique. Inst. Fr. Pondichéry – Trav. Sect.
Eocene succession of Ajire-1 well, Anambra basin. Sci. Tech. 19: 11–92.
Proc. 20th Annual Meeting of the AASP. Ulloa U.C., Nickrent, D.L., Whitefoord, C., Kelly, D.L. 2010.
Malécot, V., Schatz, G.E., Bosser, J. 2003. Révision synop- Hondurodendron, a new monotypic genus of Aptan-
tique du genre Phanerodiscus Cavaco (Olacaceae) à draceae from Honduras. Ann. Missouri Bot. Gard. 97:
Madagascar. Adansonia III, 25: 119–128. 457–467.
Coulaceae
Coulaceae Tiegh., Bull. Mus. Hist. Nat. 1: 168 (1897).
Olacaceae subfam. Dysolacoideae Engler, tribe Couleae Engler (1897).
Trees with alternate, petiolate leaves, venation 2. Inflorescence branched; stamens mostly in 3 series, one
pinnate; schizogenous resin ducts and laticifers alternating with petals and two opposite petals;
present in all parenchymatous tissues; indumen- W Africa 1. Coula
tum of short, branched, brownish hairs on most – Inflorescence simple; stamens 3 opposite each petal;
Borneo, Sumatra, and some adjacent areas
young parts. Inflorescence an axillary, simple or 3. Ochanostachys
compound spike. Flowers bisexual, sessile or
nearly so; calyx small, shallowly lobed, not
accrescent in fruit. Petals mostly 5, distinct or
basally connate, adaxially glabrous or partly GENERA OF COULACEAE
hairy; stamens in 1–3 whorls, distinct or (Min-
quartia) epipetalous, one whorl opposite the 1. Coula Baillon Fig. 8
petals, one alternating with them, and the third
(when present, Coula) between them and twice as Coula Baillon, Adansonia 3: 64, t. 3 (1863).
many; anthers basifixed, short-globular. Ovary
superior, broadly conical, short-hairy; style very Trees with alternate, coriaceous, petiolate leaves,
short, stigma 2- to 4-lobed, ovary with 4 locules young parts with short, brownish epidermal
confluent above, each locule with one pendent, hairs. Inflorescences axillary, compound spikes.
unitegmic or bitegmic ovule. Fruit a small, one- Flowers bisexual, sessile or nearly so, calyx a very
seeded; cotyledons (2) 3 or 4. short and smooth rim, petals 4/5, distinct;
A family of three monotypic genera, one in stamens 12–20, in 3 whorls, the outer whorl alter-
tropical America (Minquartia), a second in tropi- nate with the petals and longest, the inner whorl
cal Africa (Coula), and the third in the Indonesian opposite and shortest, and the middle one of
area (Ochanostachys). The family is characterized medium length, opposite the petals but to the
by its schizogenous resin ducts and laticifers, the left and right of their median; sometimes the
non-accrescent calyx, the often multiple series of inner whorl missing; anthers basifixed. Ovary
stamens, and the superior ovary. superior, broad, terminating in conical style
with small stigma, ovarian cavity with 3 or 4
lobes below, simple above, where 3 or 4 ovules
KEY TO THE GENERA OF COULACEAE pendent from a central funiculus. Fruit a globular
drupe with abundant endosperm and small, dico-
1. Inflorescence a simple spike bearing small cymes; tylous seedling.
corolla campanulate; stamens in 2 series, alternating One sp., Coula edulis Baillon, tropical Africa.
with and opposite petals, epipetalous at mid-height of
the corolla; Nicaragua and southwards 2. Minquartia 2. Minquartia Aubl. Fig. 9
– Inflorescence simple or branched, but flowers not in
cymes; corolla not campanulate; stamens in 2 or 3 Minquartia Aubl., Hist. Pl. Guian., Suppl. 4, t. 370 (1755).
series, not or scarcely epipetalous; paleotropics 2
66 Coulaceae
Fig. 9. Coulaceae. Minquartia guianensis. A Branch with

Fig. 8. Coulaceae. Coula edulis. A Flowering branch. B flowers and immature fruit. B Part of inflorescence. C Part
Bud. C Flower. D Petal. E Stamens, left from ventral, right of corolla, inside, with stamens. D Calyx and ovary. E
from side. F Flower with anterior petals and stamens Same, longitudinally sectioned. F Mature drupe. G Same,
removed. G Pistil longitudinally sectioned. H Transverse longitudinally sectioned. (Sleumer 1984a)
section of pistil. I Fruit and seed, longitudinally sectioned.
(Engler 1915)
Tree with milky juice and hard, white bark, usu- of the corolla, 5 opposite the petals and 5 alter-
ally with basal buttresses. Leaves alternate, nating with them, filaments filiform; anthers 4-
entire, petiolate, venation pinnate, blade ellipti- locular, dehiscent longitudinally. Ovary hairy,
cal with long tip, glabrous above, somewhat (3)4(5)-loculate below and simple above; ovule
rusty-haired and glabrescent below; indumen- one anatropous, bitegmic, attached to a central
tum stellate; secretory cavities present with res- funiculus, pendent from the central placenta in
inous contents as well as laticifers and “spicular each partition; style very short, stigma sessile,
cells”. Inflorescence a generally simple, shortly 3–5-lobed. Fruit a small, ovoid drupe with thin,
pedunculate, axillary spike, with scales each sub- fleshy exocarp with latex and hard endocarp,
tending a nearly sessile cyme with essentially with one seed; endosperm ruminate.
sessile, bracteate, bisexual flowers. Calyx small, One sp., Minquartia guianensis Aubl., Nicar-
persistent, 5-(6-)toothed, not accrescent. Petals agua southwards, to Brazil, Peru, and Bolivia.
4–7, connate for the lower half, fleshy, campan- 3. Ochanostachys Mast. Fig. 10
ulate, the distinct lobes adaxially hairy. Stamens
mostly 10, sometimes 15, connate with the base Ochanostachys Mast. in: Hook., Fl. Brit. Ind. 1: 576 (1875).
References 67
Trees, said to be autotrophic (Ping 1997). Young

parts with short, rust-colored epidermal hairs.
Leaves alternate, coriaceous. Inflorescence a
long, axillary spike. Flowers bisexual, with small,
cup-shaped calyculus. Petals 4 or 5, essentially
distinct. Stamens 12–15, 3 opposite each petal,
anthers globular. Ovary thick, short, conical,
incompletely 3-loculed, with 3 ovules pendent
from the tip of a central funiculus. Fruit a drupe
with thin exocarp and woody endocarp.
One sp., Ochanostachys amentacea Mast.,
Indonesia and some adjacent areas.
References
Engler, A. 1915. Die Pflanzenwelt Afrikas. III, 1. Leipzig:
W. Engelmann.
Ping, S.T. 1997. Root hemi-parasitism in Malayan Olaca-
ceae. Gardens Bull. Singapore 49: 1–13.
Sleumer, H. 1984a. Olacaceae. Flora Neotropica 38: 1–159.
New York: Organiz. For Fl. Neotrop.
Sleumer, H. 1984b. Olacaceae. Flora Malesiana, I, 10: 1–29.
Fig. 10. Coulaceae. Ochanostachys amentaceae. A Flower-

ing branch. B Flower bud. C Flower with 2 petals removed.
D Fruit. (Sleumer 1984b, drawn by J. van Os)
Eremolepidaceae
Eremolepidaceae Tiegh. ex Nakai, Bull. Natl. Sci. Mus. 31: 48 (1952); Kuijt, Syst. Bot.
Monogr. 18: 1–60 (1988), rev.
Small, mostly glabrous parasites, often on Myrta- they are opposite; juvenile Eubrachion plants
ceae, some species with epicortical roots bearing also have opposite, somewhat acicular leaves,
secondary haustoria. Leaves alternate or oppo- later shoots abruptly forming squamate-peltate
site, simple, entire, exstipulate, squamate leaves that are alternate. Inflorescences bear
in mature Eubrachion. Inflorescence a small, scale leaves that may be caducous, at least the
indeterminate spike or raceme, sometimes cat- upper ones subtending flowers. The bud scales
kin-like, mostly axillary, subtended by usually of Lepidoceras are distinctive in having acute,
caducous scaly bracts. Flowers monochlamydous, sclerotic tips; they are especially unusual in the
unisexual, mostly sessile, ebracteolate; plants female, where they resume growth to form pho-
dioecious or monoecious. Staminate and pistil- tosynthetic leaves that retain the sclerotic apical
late flowers 2–4-merous, petals small or (Anti- tooth from the original bud scales.
daphne amazonensis, A. viscoidea) lacking; No information is available on the anatomy of
stamens distinct, opposite petals, anthers 4-locu- shoots or leaves, except for a brief developmental
late, filaments often very short. Pollen echinate study of the squamate leaves of Eubrachion
(shallowly reticulate in Eubrachion), tricolporate (Bhandari 1969).
or porate, oblate-spheroidal. Ovary partly or
entirely inferior, style short and stout, stigma INFLORESCENCES. Inflorescences are spike-like or
capitate. Fruit a 1-seeded berry, in color ranging racemose, axillary in all species except in female
from green through ocher or reddish to black. Lepidoceras, where an inflorescence is absent
Seed with abundant, whitish to light green endo- (unless each leafy shoot is so visualized), the
sperm, this absent in Lepidoceras; embryo dico- solitary flowers being subtended by foliage leaves.
tylous (acotylous in Lepidoceras peruvianum). In two species of Antidaphne (A. glaziovii and A.
A strictly American family of three small viscoidea), however, the tip of the female inflores-
genera of ramal parasites, several with striking cence retains a few arrested foliage leaves that,
epicortical roots, mostly alternate phyllotaxy upon the elongation of the young infructescence,
and small, unisexual flowers. Together the may resume growth and expand into small foliage
approximately dozen species range from Chiapas leaves. The male inflorescence of the rare A. ama-
to N Argentina, Uruguay, and southern Chile zonensis is highly aberrant and may be teratolog-
(Chiloé), with minor representation on the ical. In A. andina, flowers of both sexes are
Greater Antilles, in Venezuela, Colombia, and sessile, and we can scarcely speak of an inflores-
Ecuador. Molecular data have led recent workers cence.
(Nickrent et al. 2010) to include the family as a
separate clade in Santalaceae. FLORAL MORPHOLOGY. Flowers of Eremolepidaceae
are very small, unisexual (without aborted organs
VEGETATIVE MORPHOLOGY. The leaves are alternate of the opposite sex), monochlamydous, with 2–4
in all mature plants except Lepidoceras, where petals; in A. punctulatum, both types of flowers
70 Eremolepidaceae
are 3-merous, as usually are pistillate A. viscoidea HAUSTORIAL CONNECTION. Haustorial attachments
flowers. Stamens are extremely small, 4-loculate, in the family have not been investigated anato-
the filaments very short except in some Anti- mically. In Eubrachion and Lepidoceras, the
daphne. A glandular cushion occupies the center haustorium is a morphologically simple, knob-
of the staminate flower. The ovary is basically like structure, no epicortical roots being formed.
inferior, but in A. viscoidea it is semi-inferior. In at least Antidaphne viscoidea, however, the
Little is known of the inner structure of the primary haustorium may become a large, sad-
ovary but we may assume that, as in Eubrachion, dle-shaped structure, in its early stages being
there exists a central ovarian cavity with a papilla- associated with sparsely branched epicortical
like basal emergence containing several embryo roots bearing conspicuous secondary haustoria.
sacs. No other embryological studies exist in the These roots eventually die off from the tips
family. The absence of endosperm in Lepidoceras towards the base of the plant, the nearest second-
seeds is likely to mean re-absorption of the pro- ary haustoria fusing with the primary one to
ducts of fertilization of the endosperm nucleus. become a large, compound organ (Kuijt 1964).
Several other Antidaphne species are known to
POLLEN. Pollen in the family is tricolporate or have epicortical roots; in A. wrightii, individuals
colpate and oblate-spheroidal, in Antidaphne without such roots may also be encountered
and Lepidoceras with echinate morphology while (Kuijt 1988).
Eubrachion has a depressed-reticulate pollen sur-
face without spines (Feuer and Kuijt 1978). KARYOLOGY. The number of chromosomes varies
even within Antidaphne, where A. viscoidea has
POLLINATION. Pollination has not been studied in n ¼ 13 but A. andina has n ¼ 10. The approxi-
Eremolepidaceae, but numerous small, stingless mate count in Lepidoceras (n ¼ ca. 11) needs
bees have been observed visiting the staminate confirmation (Wiens and Barlow 1971). Chromo-
flowers of A. viscoidea (Costa Rica; pers. obs.). somes are unusually small, in contrast to those of
most Loranthaceae and Viscaceae.
EMBRYOLOGY. Embryological studies have been
carried out only in Eubrachion (Bhandari and PHYLOGENY. The genera of Eremolepidaceae have
Indira 1969). As in nearly all mistletoes, there is traditionally been placed in Loranthaceae sub-
a single ovarian cavity with a small basal ovarian fam. Viscoideae (now Viscaceae), but recent
papilla. Within it, 1–3 megaspore mother cells molecular information points to closer affinities
differentiate. Development proceeds according to (even inclusion in) the Santalaceae—in South-
to the Allium type, with eight nuclei, the egg East Asia, the latter also contain some branch-
apparatus being placed at the distal pole of the parasitizing taxa (Vidal-Russell and Nickrent
greatly elongated embryo sac. Only one embryo 2008; Nickrent et al. 2010) that have evolved sep-
sac is functional, the others degenerating. Double arately from, and later than, Eremolepidaceae.
fertilization follows, including the formation of a Not denying such possible relationships, I have
cup-shaped body of endosperm clasping the argued (Kuijt 1968) for a continued separation at
eventually bicotylar embryo. A multicellular sus- the familial level both from Viscaceae (itself
pensor pushes the young embryo into this endo- included in Santalaceae by APG 1998 but not by
sperm. No endosperm is formed in Lepidoceras, Nickrent et al. 2010), and from Santalaceae.
and it is not known if double fertilization occurs. Molecular work has documented that the aerial
parasitism is of a different origin than that of
FRUIT AND SEED. As in nearly all mistletoes, the fruit other aerial Santalaceae; cork cambium is present
is a one-seeded berry in which the (poorly demar- in Eremolepidaceae but is said to be absent in
cated) seed is surrounded by a mass of viscin tissue. Santalaceae. The Santalacean flora of South and
In Antidaphne, it has copious whitish to light green especially Central America is very sparse. The
endosperm. The embryo is dicotylous, acotylous in family thus represents a unique, purely American
Lepidoceras peruvianum (Kuijt 1982). evolutionary experiment.
GENERA OF EREMOLEPIDACEAE 71
KEY TO THE GENERA OF EREMOLEPIDACEAE
1. Leaves of adult plants squamate and peltate

2. Eubrachion
– Leaves of adult plants foliaceous, mostly petiolate 2
2. Epicortical roots often present; leaves of adult plants
alternate, mostly without sclerotic tooth; endosperm
present; southern Chile to Chiapas and the Greater
Antilles 1. Antidaphne
– Leaves of adult plants opposite, each terminating in a
sclerotic tooth; endosperm absent; southern Chile or
Ayacucho 3. Lepidoceras
GENERA OF EREMOLEPIDACEAE
1. Antidaphne Poepp. & Endl. Fig. 11
Antidaphne Poepp. & Endl., Nov. Gen. Sp. Pl. 2: 70 (1838).

Eremolepis Griseb. (1838).
Leafy plants with alternate phyllotaxy even when

young; stems terete to somewhat angular, smooth
or verrucose; basal epicotylar roots with secondary
haustoria present in at least some, perhaps all
species; primary haustorium becoming very large
and saddle-shaped at least in A. viscoidea, eventu-
ally incorporating the nearest secondary haustoria,
when root tips and distal secondary haustoria die Fig. 11. Eremolepidaceae. Antidaphne viscoidea. A
back. Leaves (ob)lance-elliptic to nearly orbicular; Young shoot. B Leaf of “orbicularis type”. C Flowering
lower portions of innovations with small, caducous shoot. D Pistillate inflorescence. E Staminate inflores-
cence. (Kuijt 1981, drawn by author)
scale leaves. Monoecious, inflorescences unisexual
or gynoecandrous (staminate flowers below, pistil-
late ones above) or essentially absent or dioecious; widely (Chiapas to Bolivia); A. wrightii, on
inflorescences generally few-flowered and with Cuba, Hispaniola, and Puerto Rico, is exceedingly
caducous scale leaves. Staminate inflorescence a rare or locally extinct. Some plants have epicor-
spike or raceme (except for the perhaps teratologi- tical roots, others not, and the compound inflo-
cal A. amazonensis), staminate flowers mostly 3- or rescence of some is not known elsewhere.
4-merous, apetalous or not, with central glandular
disk; stamens 3 or 4, opposite petals and distinct, 2. Eubrachion Hook. f.
anthers 4-loculate. Female spike of some species
with 2 or more arrested leaves near the tip, these Eubrachion Hook. f., Fl. Antarct. 2: 291 (1846).
and the infructescence axis expanding following
anthesis; in other species, 1 or 2 pistillate flowers Rigid, erect, sympodial plants, with globular, sim-
sessile near the base of short staminate spike; pis- ple, knob-like primary haustorium, lacking epi-
tillate flower 2–4-merous, with small, triangular cortical roots. Juvenile plants with linear, acute,
petals, persistent or not; ovary inferior or semi- paired leaves; mature plants with peltate, squa-
inferior (or style basally swollen), stigma capitate- mate, alternate leaves, each with blackish to
cristate. Fruit a variously colored berry, endo- brown margin, eventually deciduous. Inflores-
sperm copious, creamy white to light green; cence simple or (one sp.) in terminal, compound
embryo dicotylous. n ¼ 10, 13. arrangement; inflorescence units spicate, gynoe-
Eight spp., ranging from Chiapas to Brazil candrous or female. Staminate flowers subtended
and Chile (Chiloé), only A. viscoidea ranging by caducous, pistillate by persistent scale leaves,
72 Eremolepidaceae
the staminate with 3 or 4 petals and stamens, the Erect plants, shoots glabrous or with soft,
pistillate with 3 or 4 petals, ovary inferior. Seed stout hairs, with globular, simple primary haus-
with cup-shaped endosperm. torium; epicortical roots absent; internodes
Two spp., one in Venezuela and (rarely) in terete. Leaves opposite. Dioecious or monoe-
Colombia and Ecuador, the other one from Uru- cious. Staminate inflorescence an axillary raceme
guay and northern Argentina to south-eastern with caducous scale leaves. Petals 4, with central,
Brazil, with isolated occurrences on Jamaica and glandular disk. Pistillate flowers solitary in leaf
(very rarely) Hispaniola and Puerto Rico. axils, 4-merous, ovary cylindrical, the short style
arising from a disk-like base. Fruit with short
3. Lepidoceras Hook. f. Fig. 12 stalk. Seed lacking endosperm, the embryo dico-
tylous or acotylous and globular, blue or brown-
Lepidoceras Hook. f., Fl. Antarct. 2: 293 (1846). ish green. n ¼ ca. 11.
Myrtobium Miquel (1852). Two spp., one in southern Chile, the other
known from 2 collections in central Peru (Ayacu-
cho).
References
APG, 1998. An ordinal classification for the families of

flowering plants. Ann. Missouri Bot. Gard. 85:
531–553.
Bhandari, N.N. 1969. Ontogeny and marginal growth in
the leaf of Eubrachion ambiguum. Ann. Bot. 33:
537–540.
Bhandari, N.N., Indira, K. 1969. Studies in the Viscaceae.
IV. Embryology of Eubrachion (Hook. et Arn.) Engl.
Bot. Notis. 122: 183–203.
Feuer, S., Kuijt, J. 1978. Fine structure of mistletoe pollen.
I. Eremolepidaceae, Lepidoceras and Tupeia. Can. J.
Bot. 56: 2853–2864.
Kuijt, J. 1964. Critical observations on the parasitism of
New World mistletoes. Can. J. Bot. 42: 1243–1278.
Kuijt, J. 1968. Mutual affinities of Santalalean families.
Brittonia 20: 136–147.
Kuijt, J. 1981. Inflorescence morphology of Loranthaceae
- an evolutionary synthesis. Blumea 27: 1–73.
Kuijt, J. 1982. Seedling morphology and its systematic
significance in Loranthaceae of the New World,
with supplementary comments on Eremolepidaceae.
Bot. Jahrb. Syst. 103: 305–342.
Kuijt, J. 1988. Monograph of the Eremolepidaceae. Syst.
Bot. Monogr. 18: 1–60.
59: 538–558.
Vidal-Russell, R., Nickrent, D.L. 2008b. The first mistle-
toes: origins of aerial parasitism in Santalales. Molec.
Fig. 12. Eremolepidaceae. Lepidoceras chilense. A Habit Phylogen. Evol. 47: 523–537.
of female plant in fruit. B Sclerotic leaf tip. C Staminate Wiens, D., Barlow, B.A. 1971. The cytogeography and
inflorescence. D Bud of staminate inflorescence. E Pistil- relationships of the viscaceous and eremolepidac-
late flower. F Fruit. (Original J. Kuijt) eous mistletoes. Taxon 20: 313–332.
Loranthaceae
Loranthaceae Juss., Ann. Mus. Hist. Nat. Paris 12: 292 (1808) (‘Loranthaea’), nom. cons.; Barlow, Flora Males. I, 13:
209–401 (1997); Polhill and Wiens, Mistletoes of Africa, Royal Bot. Gard. Kew (1998).
Loranthaceae subfam. Loranthoideae Eaton, Bot. Dict., ed. 4: 37 (1836).
Elytranthaceae Tiegh. (1896).
Nuytsiaceae Tiegh. (1896).
Gaiadendraceae Tiegh. ex Nakai (1952).
Psittacanthaceae Nakai (1952).
Perennial plants, brittle, parasitic mostly on the of Passovia, petals alternating with fertile stamens
branches (rarely, roots) of woody dicotyledons, and staminodia; anthers basi- or dorsifixed-versa-
infrequently on Gymnosperms, shrub-like (in 3 tile, tetrasporangiate and/or bisporangiate, some-
cases terrestrial or frequently terrestrial shrubs or times with transverse septa or alveolar; sepals
trees parasitizing roots of hosts), glabrous or reduced to a calyculus; ovary inferior, crowned
(especially in the Old World) with complex hairy by an entire to dentate (rarely fissured) calyculus,
surface; shoots percurrent, sometimes dichoto- with a single, sometimes lobed ovarian cavity, the
mous in Aetanthus and Psittacanthus; haustorial number of carpels not known; ovules absent, usu-
attachment single, occasionally very large, in ally replaced by a single, central, basal ovarian
many genera accompanied by epicortical roots papilla giving rise to several aggressively growing
bearing secondary haustoria, primary haustorium embryo sacs. Fruit a one-seeded berry, the endo-
lacking in terrestrial genera; epicortical roots sperm-embryo complex partially or entirely envel-
rarely giving rise to aerial shoots; one or two oped by a layer of viscin; endosperm abundant in
(Chilean) spp. sprouting from within host tissues. all but two neotropical genera (Aetanthus and
Leaves petiolate to sessile, estipulate, usually Psittacanthus) where the embryo is massive; coty-
paired, occasionally whorled, alternate, or irregu- ledons 2 (to 12 in some Psittacanthus), cotyledon
lar, entire, thin to coriaceous or fleshy, lacking tips distinct or connate; radicular pole frequently
altogether in one or two species, very rarely sea- swollen and eventually producing the endogenous
sonally deciduous. Inflorescences determinate or intrusive organ. n ¼ 12.
indeterminate, a (sometimes compound) spike, About 77 genera and 950 spp., mostly tropical
raceme, or umbel, terminal or axillary or both, and subtropical, rarely reaching the temperate
mostly made up of lateral monads or triads sub- zones, with several centers of diversity: tropical
tended by bracts and with or without prophylls; America, Africa, tropical Asia, and New Zealand-
very rarely flowers solitary and sessile or pedicel- Australia. All genera are limited to either the Old
late in leaf axils. Flowers bisexual in most genera, or the New World, with no close relationships
unisexual and plants dioecious in some, and very between the two groups except in the Atkinsonia-
rarely monoecious; flowers actinomorphic to Gaiadendron-Nuytsia trio of primitive genera.
zygomorphic (Old World), 4–8-merous; petals
choripetalous, or sympetalous in some African V E G E T A T I V E M O R P H O L O G Y . Loranthaceae are
genera (and in Cladocolea biflora in Mexico), espe- mostly small to medium-sized, brittle mistletoes
cially in the Neotropics often somewhat dimorphic semiparasitic on branches of woody plants,
in size; stamens as many as petals, epipetalous, monocots being avoided almost entirely and
anthers sometimes sessile, dehiscence introrse or only a few species parasitizing Gymnosperms.
latrorse; stamens dimorphic in many American The formation of epicortical roots occurs in
genera but generally isomorphic in the Old many genera of both the Old and New Worlds.
World; in one genus (Dendropemon) and 2 spp. Such roots develop from the external part of the
74 Loranthaceae
primary haustorium, and in some neotropical bearing crystals, and stellate sclereids. The taxo-
genera also from the branches when in contact nomic importance of the last cell type also
with other, nearby branches. Leaves are simple, received further support for Peristethium, where
estipulate, with entire margins, perennial except an extreme example is P. roraimense, in which
in Desmaria mutabilis, Loranthus europaeus, and most of the leaf mesophyll has differentiated into
two South African species of Tapinanthus that are stellate sclereids. Desmaria is unique in having
deciduous (Kuijt 1985). numerous, long, slender, serpentine fibers
throughout the mesophyll area. Unfortunately,
B R A N C H I N G P A T T E R N S . Shoots are percurrent no comparable data are available for the Lor-
in the majority of Loranthaceae, innovations usu- anthaceae of the Old World.
ally originating in the axils of lower leaves, espe-
cially where terminal inflorescences characterize I N F L O R E S C E N C E S . The structure of the inflores-
a species. In some genera, however, the shoot cence in Loranthaceae provides significant taxo-
apex aborts following the formation of one or nomic information and often gives insights into
more pairs of leaves, new growth being initiated evolutionary relationships. This is true even in
in the most distal leaf axils. A dichotomous their complete absence, as in the American
branching pattern thus results; there are numer- genus Phthirusa, where the flowers are individu-
ous examples of this in Psittacanthus and ally sessile in the foliar axils, often clustered, and
Aetanthus. When one of the two resulting inno- each is flanked by prophylls. This is held to be a
vations becomes dominant, a deceptive situation primitive feature, and is different from the single,
may follow where that innovation appears to be pedicellate flowers of Ligaria and some tropical
percurrent, as has been pointed out in Amyema species, as in Sogerianthe, which seem to repre-
(Kuijt 1980a) and also occurs in Psittacanthus sent reductional end-points.
(Kuijt 2009a). A modification of this dichoto- There have been two major efforts to place
mous branching is seen in species with whorled the diversity of inflorescences in an evolutionary
phyllotaxy, where trichotomies occur, as in context and, while there was agreement on struc-
Aetanthus trifolius (Kuijt 2009b). In Desmaria tural facts, the focus in these two studies diverged
mutabilis and Psittacanthus palmeri, lateral radically. In the first, a study that dealt with the
short shoots have evolved that bear the flowers. extremely diverse genus Amyema, reduction is
emphasized as an evolutionary trend, leading
S T E M A N A T O M Y . Surprisingly little is known from complex inflorescences to progressively
about the anatomical structure of the stems of simpler ones (Barlow 1966). In the second (Kuijt
Loranthaceae. Carlquist (1985) briefly refers to 1981), the opposite is true: beginning with the
the vessels with laterally widened pits and the simplest condition (the absence of inflorescences
presence of thick-walled fibers in the wood of a as mentioned above) it provides a scheme of
species of Psittacanthus, and the absence of elaboration to reach more complex inflores-
growth rings in that species. However, Gómez- cences; however, reductional events are not
Sánchez et al. (2011) have provided a detailed denied. There remain curious inflorescences that
description of two Mexican species. are difficult to explain under either scheme, such
as the umbellate inflorescence tetrads in some
F O L I A R A N A T O M Y . The occurrence of foliar Amyema species that carry a sessile flower in
sclerenchyma as a taxonomic character was first the middle, as in A. pendula and the remarkable
emphasized in Oryctanthus (Kuijt 1961), where A. dilatipes (see Kuijt 1981, his Figs. 24 and 25).
so-called stellate fiber bundles were thought to be According to the “progressive” evolutionary
diagnostic of the genus. In a more recent and scenario, the single axillary flower as seen in
more comprehensive survey, it was discovered Phthirusa evolved a stalk, its two prophylls fusing
that similar structures are present also in one or with it and subtending two more flowers, a simple
two Struthanthus species; however, its taxonomic dichasium as in the primary inflorescences of
importance in Oryctanthus was also clearly con- Cladocolea dimorpha. The next evolutionary
firmed by Kuijt and Lye (2005a). In the same development would see an elongation, and addi-
paper, many new observations were recorded on tion of more paired flowers, a condition produc-
other types of sclerenchyma, especially those ing the determinate inflorescences exemplified by
Loranthaceae 75
many extant Cladocolea species. The addition of F L O R A L S T R U C T U R E . The flowers of Lorantha-

prophylls to each lateral flower, and the loss of ceae are exceedingly diverse in size, morphology,
the terminal one, results in an inflorescence type and color schemes, especially in Africa (Kirkup
presently seen in a number of genera in both the 1998; Polhill and Wiens 1998), undoubtedly
Old and the New World, as in Dendropemon, reflecting the variety of pollination mechanisms
Panamanthus, and some paleotropical genera. in the family. Floral elements are inserted on an
(In Dendropemon and Panamanthus, the floral inferior ovary crowned by a rim of tissue called
prophylls fuse with the primary bract to form a the calyculus. It is variable in prominence and
cupule clasping the base of the ovary.) From ranges from inconspicuous and essentially
there, the evolution of flowers (sessile or pedicel- smooth to strongly dentate as, for example, in
late) in axils of prophylls is but a small step, as Aetanthus mutisii and the recently discovered
achieved in Passovia and Struthanthus, but also Gaiadendron coronatum, and mostly persists in
approximated in some Old World genera like the fruit. The calyculus has, in the past, been
Diplatia and Dicymanthes. One of the appealing controversial but is now generally accepted as a
aspects of this evolutionary scheme is the fact that reduced calyx; its vasculature is poorly or not
all intermediate stages can be seen in extant documented in most cases, but vascular traces
genera or species in the Americas; see, for exam- are reported for Atkinsonia, Gaiadendron punc-
ple, the various species of Peristethium (Kuijt tatum, and Nuytsia (Narayana 1958; Nickrent
2012). In many species of Amyema (e.g., A. gib- et al. 2010). In some other Santalalean families
berula), and in all species of Aetanthus, the like Aptandraceae, the mature calyculus is very
median flower of lateral triads has dropped out large and profusely vasculated. It constitutes one
to provide dyads. I consider that nearly all lor- of the reliable contrasts between Loranthaceae
anthaceous inflorescences can be accommodated and the other large mistletoe family, Viscaceae,
following this scheme, with the above-mentioned where it is completely absent. As mentioned pre-
puzzling exception(s). viously, Wanntorp and Ronse de Craene (2009)
One further phenomenon that remains to be have a different view of the floral organs of Lor-
mentioned is the fact that in several Psittacanthus anthaceae, and especially of the calyculus, and
and Aetanthus species, inflorescences emerge not regard the latter as a modification of prophylls.
only in axillary positions but also endogenously It is impossible, among other things, to harmo-
all around the node. In the paleotropical Lepeos- nize this view with the occurrence of clearly
tegeres and Cyne, the axillary inflorescence is defined prophylls where occurring in addition to
completely encased in a capsule of cork that the standard calyculus, as in genera like Oryc-
needs to be breached for the inflorescence to tanthus, Maracanthus, and Oryctina (Kuijt 2013).
emerge. In a much more inconspicuous fashion, Petals in Loranthaceae are valvate and range
this is also true for the inflorescences of some from 4 to 7(8), generally being choripetalous, but
Mexican species of Cladocolea (Kuijt 1975), and their lowest portions frequently adhere during
suggestive corky craters are seen around the base anthesis and may give the impression of a con-
of many other axillary inflorescences in Lor- nate floral tube. This cohesion is sometimes aided
anthaceae like those of Ileostylus and Peraxilla. by interlocking marginal teeth or trichomes. In
Dactyliophora has some of its inflorescences some African species, the petals are genuinely
emerge in this endogenous fashion from epicor- concrescent basally, the mesophyll of adjacent
tical roots. In some Amyema species, individual ones being confluent (Kirkup 1998), but in the
flowers are produced endogenously at the foliar majority of Loranthaceae the corolla is choripe-
nodes (Kuijt 1980a). A similar phenomenon is talus. In the remarkable, extremely rare Cladoco-
present in Misodendraceae. lea biflora from southern Mexico, which has a
Compound (i.e., branched) inflorescences campanulate flower, we find an indisputably
have developed regularly in some species of gamopetalous flower as the sole known neotropi-
Passovia and Oryctanthus, and (rarely) in cal example (Kuijt 1980b). Atkinsonia is said to
Struthanthus and in Dendropemon (Kuijt 2011a). be gamopetalous by Nickrent et al. (2010), but
76 Loranthaceae
Barlow (1966) writes that it is choripetalous. Sev- dehiscing with a single longitudinal slit (Taxillus
eral paleotropical genera, also in Africa, indisput- cuneatus, Bhatnagar and Johri 1983, and several
ably have petals connate at the base, such as genera in Africa). In some Psittacanthus, pollen
Lepeostegeres, Lampas, and Lepidaria. Wanntorp sacs are distinctly alveolate, opening with numer-
and Ronse de Craene (2009) have advanced the ous small pores, for example in P. baguensis and
notion that Loranthaceous flowers have two P. crassifolius. Cladocolea biflora is peculiar here,
series of perianth members (3 petals and 3 too, in that the anther has two rounded clusters of
sepals), but this cannot apply to the numerous apertures releasing the pollen. Frequently, the tip
taxa that have 5 perianth members; it also can of the anther bears a connectival horn or protu-
scarcely be true for Cladocolea biflora, in which berance, the extreme being the needle-like apex
the perianth is connate, or for the paleotropical characteristic of Aetanthus and one species of
genera where this is also true. Psittacanthus, P. hamulifer (Kuijt 2009a).
Petals are mostly glabrous both inside and Filaments are usually slender, except in
outside, but the Old World shows exceptions in small-flowered neotropical genera like Passovia
both regards, the former exceptions being very and Dendropemon. They are partly connate with
rare. In tropical America, petals are also usually the subtending petal, as shown by a raised ridge
glabrous externally, with rare exceptions such as leading downwards. Especially in some neotropi-
in Psittacanthus lasianthus and P. pilanthus. The cal genera like Passovia, Phthirusa, and Peri-
same genus has numerous species where, mostly stethium, but also in some Psittacanthus species,
at the filament-petal junction, we find long, stiff, anthers are sessile in the upper portions of the
shiny hairs of unknown function; in rare cases, corolla.
hairs are present on filaments or on the backs of Stamen dimorphism (placed at two different
anthers (Kuijt 2009a). Here the Mexican Cladoco- heights) appears to be almost exclusively a New
lea biflora again requires being mentioned, as its World feature, where it is encountered in nearly
petals, behind the anthers, bear a conspicuous fan every genus. In some dioecious species of Passo-
of stout, beaded bristles. The occurrence of hairs via and Maracanthus, we may speak of a double
behind the anthers is usually considered a Santa- dimorphism, as the staminate and pistillate flow-
laceous feature (Nickrent et al. 2010), although it ers, of course, have very different anthers. A few
occurs elsewhere occasionally. instances of stamen trimorphism are known in
In a separate category are the surface modifi- Psittacanthus, as well as in Gaiadendron puncta-
cations of the petal’s inner surface. These were tum (Kuijt 2010).
extensively explored in the early work of Balle A special type of anther, the “Passovian
(1955) on African Loranthaceae. In many of anther”, is known from Dendropemon and a clus-
those species, there are longitudinal folds or ter of species of Passovia. Here the (dorsifixed)
ridges, especially on the lower parts of the petals. filament is flattened and forms a centripetal
Basal ligules are not frequent in Africa, but very median flange that separates two longitudinal
common in Psittacanthus. These structures may depressions accommodating the pollen sacs of
be strap-like or tongue-like; in some species, they the adjacent, much shorter stamens. In the for-
are covered with papillate hairs. The function of mer genus, the longer series of stamens is sterile,
ligules has not been established, but presumably a feature that has independently also arisen in at
is related to nectar production or retention. least two species of Passovia (Kuijt 2011b). Also
Anthers in Loranthaceae may be dorsifixed- in Passovia, the size and shape of the connectival
versatile or basifixed, examples of each being horn varies greatly, the most remarkable case
common in both the Old and the New World; being P. ensifera where each anther (including
very rarely, they are sessile. The number of pollen the sterile ones) is topped by a sword-like con-
sacs is commonly four but, especially in some nectival extension.
small-flowered genera, some anthers may have An entirely different form of anther, also
only two. Frequently the anthers are long and unique in the family, is diagnostic for the neo-
narrow; in many such cases, pollen sacs are trans- tropical genus Aetanthus. The anther consists of
versely septate, and these septa may or may not four exceedingly long and narrow thecae, being
disappear at the shedding stage, the pollen sac so narrow that it is difficult to distinguish from
Loranthaceae 77
the supporting filament. The tip of the anther reduced. It consists of an ovary wall terminating
consists of a prominent needle-like extension of in a calyculus, and its center is mostly occupied
unknown function (Kuijt 1983, 2014a). by a single (sometimes basally lobed) cavity from
Kirkup (1998) has provided a detailed analy- the base of which usually extends an ovarian
sis of the remarkable stamen evolution in many papilla or mamelon. Even the ovarian papilla is
African Loranthaceae. A number of genera (e.g., sometimes absent, having apparently merged
Helixanthera and Plicosepalus) have standard with the basal tissues of the ovary, megaspores
anthers, but in the great majority the flower differentiating in the ovarian base. The absence of
opens explosively when a bird inserts its beak an ovarian cavity itself is reported for Passovia by
into one of the preformed fenestrae of the corolla. Kuijt and Weberling (1972), but this requires
This allows the stamens to flex or coil suddenly, confirmation; it would parallel the situation in
casting pollen onto the pollinator. some species of Viscum (Viscaceae; Zaki and
Styles in Loranthaceae tend to be slender and Kuijt 1994, 1995).
only slightly shorter than the petals, bearing a What have frequently been reported to be
stigma of various degrees of differentiation just locules in the ovary of Loranthaceae are not
above the level of the anthers at least in large- locules in the normally accepted sense of the
flowered species. Curiously, in some Phthirusa word, as they are not enclosed spaces separated
species, the base of the style is greatly swollen; from each other. Rather, they are recesses in the
in Dendropemon rostratum, what seems to be an ovary wall that are open to the center or at least
elongated stylar base (nectary?) persists in the become united distally. Their number varies, per-
fruit. In three American genera (Cladocolea, Peri- haps parallel with the number of associated
stethium, and Struthanthus) as well as in Ileosty- petals. For example, Peraxilla tetrapetala has
lus from New Zealand, curiously convoluted four such recesses and four petals (Prakash
styles exist. The convolutions persist until the 1960). Since the number of these cavities varies
style is lost after flowering. All taxa with such between genera, no meaningful conclusions can
contorted styles appear to be dioecious. The fact be derived as to the number of original carpels
that convolutions are always most strongly devel- constituting the loranthaceaous ovary. No ovules
oped in the staminate flower suggests that this or integuments are recognizable, the ovarian
phenomenon is not related to the peculiarities of papilla (mamelon) at the base of the ovarian
embryo sac behavior. cavity being regarded as an evolutionary fusion
Loranthaceous flowers are mostly bisexual— of an uncertain number of ovules.
almost exclusively so in the Old World, except for
Barathranthus axanthus, which is dioecious, E M B R Y O L O G Y . The embryology of Loranthaceae
probably Loranthus odoratus (Barlow 1997), cer- is unique in the flowering plants, but our knowl-
tain irregularities in Loranthus europaeus, Tupeia edge is based almost entirely on paleotropical
antarctica, and the apparently monoecious Nuyt- taxa (Maheshwari et al. 1957); its study has been
sia (Narayana 1958; Hopper 2010). In the New largely neglected in neotropical genera, and
World, dioecy is present in certain small-flowered appears to have been discontinued generally
taxa as well as a case of monoecy in Oryctina after the 1980s.
(Kuijt 2000) and Pusillanthus (Caires et al. An indeterminate number (1–several) of
2012). In unisexual flowers, sterile organs of the embryo sacs develop in the ovarian papilla (or
opposite sex are often present, but sometimes floral base), growing laterally into the ovary wall
unrecognizable or quite absent, as in some Peri- and upwards into the style, carrying the egg appa-
stethium (Kuijt 2012) and Passovia (Kuijt 2011b). ratus with it at the apex (see Fig. 1A above). The
Curiously, all dioecious Loranthaceae are small- development of the embryo sac of Loranthaceae
flowered. is of the Polygonum type, only the lowest one of
the four megaspores giving rise to the embryo
O V A R I A N S T R U C T U R E . The ovary of Lorantha- sac. The height to which the embryo sac advances
ceae, as in other mistletoe families, is greatly in the style varies, but seems to have a degree of
78 Loranthaceae
generic constancy (Maheshwari et al. 1957). In winged nut. The anatomical structure of fruits is
one South African species, Helixanthera ligus- complex, but has been poorly explored. The most
trina, the egg apparatus actually pushes through prominent tissue (except, usually, for the embryo
the stigmatic epidermis (Fig. 1A), and fertiliza- and endosperm) is the viscin, representing an
tion takes place there. Even more bizarre, in adhesive tissue attaching the seed to the host
Moquiniella, the embryo sac reaches the stig- surface.
matic area and curves around, its tip bearing the The viscin tissue of Passovia has been studied
egg apparatus then pointing downwards (Johri in considerable detail by Gedalovich and Kuijt
and Raj 1965; Bhatnagar and Johri 1983). The (1987), who discovered an intriguing type of his-
pollen tube grows down from the stigma to tological dimorphism suggesting a functional
accomplish fertilization of the egg cell in situ. division of labor. One tissue type consists of nar-
The proembryo is now pushed down the style row, greatly elongated cells with spirally con-
by a system of suspensor cells until it reaches structed primary walls, a cell type believed to
the ovary, where the embryo then matures. The have an adhesive function. Scattered among
most massive of such suspensors is found in such cells are clusters of large, vesicular cells
Psittacanthus (Kuijt 1967), where the actual with thinner walls; these cells are thought to con-
embryo develops from the tip of a massive tain nutritive materials important to birds. In at
multicellular body the bulk of which eventually least Psittacanthus, one end of the seedling is
collapses into a cup-shaped structure still recog- surrounded by a cap of exceedingly sticky, vesic-
nizable in the germinating seedling. ular tissue and the other end by a cap of very
Several embryo sacs compete in this curious different, elongated viscin cells (Kuijt 1973).
exercise, the proembryo reaching the ovary first There are documented instances of parent birds
suppressing slower ones, so that only one embryo feeding decorticated fruits of Loranthaceae to
matures. In these studies, the fate of the primary their young, a fact that surely confirms the pres-
endosperm cell, or its position when fertilized ence of nutrients in viscin. It is possible that
and behavior afterwards, has received inadequate observations of birds removing outer parts of
or no attention; however, it is believed that the the fruits of Dendrophthoe pentandra and D.
resultant endosperm is multiple, i.e., derived praelonga were preliminary to feeding the
from several embryo sacs. As mentioned else- young. It seems that the outer fruit tissues in
where, in two genera (Aetanthus and Psitta- cases like this, from the bird’s point of view, are
canthus), no endosperm is formed, the massive of no importance. There are other records,
cotyledons having taken over the storage func- however, of birds swallowing the fruits entire
tion. It is not known whether double fertilization (Amyema fasciculata, Scurrula ferruginea) and
takes place in these two genera, or whether it does afterwards wiping the seeds onto branches (Doc-
take place and the resultant tissues become sup- ters van Leeuwen 1954). A detailed field study by
pressed and reabsorbed. Restrepo (1987) in Colombia also warns us not to
This curious behavior of the embryo sacs of generalize too quickly, as her studies shows dif-
Loranthaceae has been known since the pioneer- ferences between birds as well as mistletoe spe-
ing studies of Treub (1881). Unfortunately, as cies. Docters van Leeuwen also presents evidence
implied above, we know nothing of the embryo- that, at least in some mistletoes, the outer fruit
logical events taking place in neotropical genera wall contains the important nutrients, while these
except for Struthanthus and Tripodanthus elsewhere are found in the outer viscin tissue. In
(Venturelli 1981, 1983). Beyond these two studies, other words, the interaction between birds and
all that is known about the bizarre behavior of mistletoe seeds is a multidimensional matter
embryo sacs is based on paleotropical genera making generalizations hazardous; no general
(Maheshwari et al. 1957). rules can be applied across the board.
Birds are the nearly exclusive dispersal agents
F R U I T A N D S E E D ; D I S S E M I N A T I O N . Fruits in of Loranthaceae; about 90 species of birds from
Loranthaceae, as in nearly all mistletoes, are 10 families are dispersal specialists. There is some
one-seeded, and fleshy, with the notable excep- suggestion that generalist dispersers are more
tion of Nuytsia, which has a dry, prominently important in carrying mistletoe seeds to
Loranthaceae 79
uninfected trees. However, there is at least one cotyledons. In Aetanthus and Psittacanthus,
obvious exception to bird dispersal. The Austra- nearly the entire seedling is made up of fleshy
lian Christmas Tree, Nuytsia floribunda, has dry, cotyledons—usually two, but in certain species
strongly alate, nut-like fruits that appear to be up to twelve. It seems that certain species, like
wind-dispersed. Since this mistletoe is a terres- P. ramiflorus and P. biternatus, may have both
trial tree, the type of bird dispersal found in other seedlings with two flat cotyledons and seedlings
mistletoes is not possible. The reported dispersal with 3 or more prismatic ones (Kuijt 1982b; R.F.
of the South American Tristerix corymbosus by Fadini, unpubl. inf.). The desert-inhabiting P.
small opossums (Amico and Aizen 2000) requires sonorae, alone in this large genus, has evolved a
corroboration, but may represent another inter- cryptocotylar germination pattern that clearly
esting exception. represents an adaptation to extreme xeric condi-
Long-distance dispersal of mistletoes has tions: a hard capsule surrounds the seedling dur-
often been mentioned in the literature, but the ing germination that is eventually broken open by
idea is usually based on present distribution pat- the expanding early leaves. Ligaria cuneifolia also
terns rather than on direct observations. Con- germinates in a cryptocotylar fashion, but its
vincing patterns are seen in several Viscaceae cotyledons remain separate (Kuijt 1982b), and
(see under that family). The Australian Mueller- eventually emerge after the endophyte is fully
ina celastroides has two documented collections established; it thus represents a transition to full
from the Bay of Islands, New Zealand, dating cryptocotyly. Most curious of all is Desmaria, in
from the 1830s, but has not been seen there which the two cotyledons are different in shape
since that time. Perhaps the most convincing and function. One cotyledon remains in the endo-
example is that of Decaisnina forsteriana (Barlow sperm to absorb its nutrients, while the other
and Schodde 1993) on remote Pacific Islands, emerges and becomes a flat, photosynthetic
documented localities being more than 1000 km organ. On the other extreme of such radical mod-
or even 2000 km apart. Another, possibly recent ifications is the primitive loranthaceous duo of
long-distance event involves the New Zealand genera (Gaiadendron, and Nuytsia) in which
Ileostylus micranthus, which has a small popula- ordinary phanerocotylar germination takes
tion on Norfolk Island. place preceding establishment of haustorial
union with host roots (Fig. 13). The number of
E M B R Y O S T R U C T U R E . The peculiar fusion of the cotyledons is usually two, but Nuytsia is mostly
cotyledonary tips of Loranthus europaeus also tricotylar or with up to 6 cotyledons (Hopper
occurs in a number of other Old World genera. 2010). The radicular pole in many genera is
In such cases, germination is cryptocotylar, the swollen even in the mature fruit, except in the
plumule emerging from between the distinct cot- trio of primitive genera with epigaeic germina-
yledonary bases. Many other genera in the Old tion (Atkinsonia, Gaiadendron, and Nuytsia), in
World show the more normal phanerocotylar which no primary haustorium is formed, and also
germination pattern that also applies to the in some branch-parasitic genera like Peristethium
majority of neotropical genera. An intermediate (Kuijt 2012).
type of cryptocotylar germination occurs in
Ligaria, where the cotyledons eventually emerge G E R M I N A T I O N A N D E S T A B L I S H M E N T . First of
when the seedling is fully established on the host. all, the germination of at least two of the three
Tristerix is the only New World genus in which terrestrial genera proceeds in a standard, phaner-
cotyledonary tips are connate. The extreme in this ocotylar fashion. In Gaiadendron punctatum it is
genus is T. aphyllus, where cotyledons are not known that the primary root swells up into a
differentiated, the seedling being a solid, tor- small fusiform tuber (see Figs. 1 or 2 in Kuijt
pedo-shaped body that can elongate to many 1963), but this does not happen in Nuytsia. The
times its original length in search of a host surface. germination of Atkinsonia does not seem to have
In overall shape, neotropical genera show been recorded except in the illustration from Bla-
much variation in their mature embryos (Kuijt kely (1922; see our Fig. 31).
1982b). Phthirusa inconspicua has a spherical After the seed of ramal mistletoes has, by the
embryo crowned by two minute, strap-shaped adhesive properties of its viscin, become attached
80 Loranthaceae
Fig. 13. Loranthaceae. Gaiadendron punctatum. A–E below it another haustorium from another plant on the
Germination sequence. F A seedling growing from side tuber. (Kuijt 1969, drawn by author)
of decaying stump of oak; above arrow an old haustorium,
to a host branch, the radicular end of the seedling enters the host tissues. The exact mechanism of
(sometimes called the hypocotyl) elongates and entry has not been clarified, but may involve a
bends towards the host in a negatively phototro- combination of mechanical forces and enzymatic
pic response, until its tip makes contact. The apex action. This curious and unexplained process is
(which is often already swollen in the mature also known in several other Santalalean families,
fruit) attaches itself by means of secretions that, especially Santalaceae (Toth and Kuijt 1976); it
at least in Passovia pyrifolia, are produced by has not been unequivocally documented in Vis-
curious, polyp-like contact cells (Dobbins and caceae where, if a similar gland develops, it is
Kuijt 1974). In the meantime, in the center of likely to be very small. Glands are present in the
the massive haustorial disk thus formed, a cluster haustoria of Atkinsonia and Nuytsia, these being
of cells enlarges and eventually dissolves the cell secondary haustoria. In the last genus, what
walls separating them, forming a small glandular seems to be comparable to an intrusive organ is
cavity filled with unidentified materials. The transformed into a double, sclerified, knife-like
future intrusive organ originates just above this organ that physically severs the stele of the host
gland, grows through it and the subjacent, inter- root. The implications of this remarkable phe-
vening cells to reach the host surface where it nomenon are not clear in terms of the physiology
Loranthaceae 81
of the haustorium except that parasitic paren- under artificial conditions for Nuytsia). The lor-
chyma enters the host xylem and presumably anthaceous mistletoes with primary haustoria
represents the path of intake of materials. require a much faster attachment to and penetra-
In Psittacanthus and Aetanthus, the seedling tion into host organs, and the viscin tissue that
consists nearly entirely of 2–12 fleshy cotyledons, surrounds the excreted seed is an essential com-
the hypocotyl-like organ being completely ponent of this process.
absent. The positioning of the voided seed is Korthals (1839) first pointed out that some
usually such that its radicular pole points Loranthaceae are phanerocotylar (for example,
obliquely towards the host. In these two genera, Elytranthe and Macrosolen) while others are
no truly terminal intrusive organ develops; cryptocotylar (Loranthus europeaus, Amyema,
instead, it is produced in the lateral flank nearest Dendrophthoe, and Scurrula, for example; Doc-
the host (Kuijt 1970, 1982b). Whether a gland is ters van Leeuwen 1954). Thus, among the branch-
part of this process is not known. parasitizing species of the Old World, the less
Cryptocotyly has also evolved in numerous specialized seedlings have two distinct cotyledons
other genera, especially in the Old World, where that withdraw from the endosperm and are pho-
such genera show a fusion of the distal cotyledon- tosynthetic organs. In the second, cryptocotylar
ary tips, leaving a basal fissure through which the type, the lower portions of the cotyledons are
first true leaves emerge (see below). Indepen- distinct, and it is through the resultant slit that
dently, the South American genus Tristerix has the first true leaves emerge. Regretfully, the seed-
evolved the same feature; in the greatly reduced lings of most Old World Loranthaceae have not
T. aphyllus, however, no cotyledons are formed, been surveyed.
the seedling being an elongated, solid, more or In the New World, the first type of germina-
less spindle-shaped body one end of which grows tion is the most common. However, in Psitta-
towards the host surface. canthus two further developments have taken
place. In a number of species, a multiplication
G E R M I N A T I O N . No special host stimuli are of cotyledons has taken place; in P. schiedeanus,
required for mistletoe germination, as demon- the number of prismatic cotyledons may reach
strated by germination of seeds on glass plates 12. It seems that in certain species, like P. rami-
when normal conditions of temperature and florus and P. biternatus, both seedlings with two
moisture are maintained. In Amyema preissii, cotyledons and those with three or more may
there are strong indications that the very high occur (Kuijt 1982b; R.F. Fadini, pers. comm.). In
CO2 concentration inside the fruit functions as a P. sonorae, a species of extreme deserts in north-
germination inhibitor (Lamont and Perry 1977), western Mexico, the viscin tissue dries into a
explaining why germination proceeds quickly as hard, tough capsule completely protecting the
soon as the pericarp is broken. Germination of germinating seedling. Its cotyledons remain in
the seed even on an acceptable host, of course, the seed and eventually shrivel up when host
does not guarantee successful establishment; it is penetration has been achieved and the first true
only on branches with a rather young periderm leaves crack the capsule open. The remarkable
that entry can be achieved. Chilean Desmaria mutabilis, as described above,
There are great differences in the germination is intermediate between phanero- and cryptoco-
behavior among loranthaceous mistletoes. tyly. It represents the only case of cotyledon
Gaiadendron, like Nuytsia and Atkinsonia, has a dimorphism in Santalales. Connate cotyledons
germination pattern like many other terrestrial also occur in the New World (Tristerix). Ligaria
plants, and does not form a primary haustorium. is essentially cryptocotylar.
Their seedlings thus have an extended indepen-
dent stage to allow their roots to make contact T H E H A U S T O R I A L C O N N E C T I O N . The attach-
with nearby host roots. The maximum duration ment structures of Loranthaceae have been
of this stage is not known; I have kept Gaiaden- explored for Africa (Calvin and Wilson 1998),
dron punctatum seedlings alive without a host for Australia (Hamilton and Barlow 1963), the New
several months, and Beyer et al. (1989) report the World (Kuijt 1964a, 1982a, 1989) and, more gen-
same for Nuytsia (Hopper 2010 speaks of 4 years erally, by Thoday (1956a, 1956b, 1958).
82 Loranthaceae
It is scarcely surprising that the haustorial

organs of mistletoes, being pivotal in their life
history, have evolved a great deal of diversity.
With some exceptions, the primary haustoria
of Loranthaceae—at least their endophytic
portions—have retained a unified, single struc-
ture, in contrast to those of the other large mis-
tletoe family, Viscaceae, where the endophyte
tends to become much fragmented. These excep-
tions are, nevertheless, of great interest.
In the mature Psittacanthus plant we cannot,
strictly speaking, refer to an endophyte at all. The
host branch is induced to form a strikingly fis-
sured, placenta-like surface to which the hausto-
rium is attached (Fig. 14). The parasite adds
successive layers of tissue to its base, the innu-
merable xylem strands below connecting to the
host xylem. In this situation, therefore, the para-
site is attached to, but not within the tissues of the
host (see Fig. 3 above). Such haustorial connec-
tions represent the largest ones in parasitic flow-
ering plants generally; in Pedistylis, they may
reach a meter in size. They are perhaps typical
of most tropical Loranthaceae.
An entirely different endophyte is known
from the New Zealand mistletoe, Ileostylus
micranthus (Condon and Kuijt 1994). The pri-
mary endophyte generated from the initial
penetrating organ develops an axial shaft that
penetrates to the host’s xylem. In successive
years, concentric lobes develop from the flanks
of the axial core, spreading out over the existing Fig. 14. Loranthaceae. Decorticated haustorial connec-
host xylem, apparently separating it from the tion of Psittacanthus ramiflorus (P) on a host branch
cambial zone, and each thus forming a shell-like (H, Quercus sp.). The host has been stimulated to
elaborate a deeply fissured woodrose, the parasite
layer. This layer during the following growth sea- adding new layers of tissue to its base (arrow). Bar ¼ 1
son is sealed off by a new increment of host wood, cm. (From Kuijt and Lye 2005a)
and the process is annually repeated, producing
several concentric shells embedded in host wood. and this appears to be true for secondary
Thus, the main active host-parasite contact haustoria also. Calvin and Wilson (1998) have
appears to be between endophytic parenchyma provided a detailed survey of these aspects in
and newly formed host xylem. Here, also, the African Loranthaceae and their host attachments.
conception of an actively penetrating endophyte However, there are cases in the family where the
is misplaced, since the endophytic lobes become endophyte undergoes fragmentation, individual
passively encapsulated. The margins of the con- cortical stands growing both acropetally and
centric flanges are irregularly lobed; no shoot basipetally into the host tissues. Loranthus euro-
production takes place from the endophyte. A paeus provides one such instance (Engler and
remarkably parallel mode of development is Krause 1935, their Fig. 51), having keel-like por-
seen in Korthalsella (Viscaceae). tions becoming embedded in the host wood and
As stated earlier, in most Loranthaceae the running parallel to the latter’s grain, just outside
haustorium is basically simple, the host wood its cambial zone, the endophytic tips being
forming a woodrose-like formation around it, pushed outwards by the action of the host
Loranthaceae 83
cambium. A cross section through the swollen much simpler haustorial connection, except that
site, that can be two or more decimeters in thick- T. corymbosus, at least on some hosts like Kagen-
ness, may show a number of such keel-shaped eckia, produces far-ranging endophytic strands
strands that have become passively embedded in from which new shoots are generated (Kuijt
the tree’s xylem. The original, primary shoot 1988). It also induces large broom-like growths
eventually dies, and is replaced by new shoots on some hosts, like poplars, again as Arceutho-
arising from nearby cortical strands. Sectional bium.
views are reminiscent of Viscacean sinkers, but No greater contrast could exist to the above
the endophytic dimorphism in that family has no than the (secondary) haustorium of Nuytsia
equivalent in Loranthaceae. In Helixanthera and (Fineran and Hocking 1983; Beyer et al. 1989).
a number of other African genera (Calvin and First of all, the two haustorial lobes that clasp the
Wilson 1998, their Fig. 1-c) further clear exam- host root grow around it, and a complete fusion
ples are present, although intraxylary portions of takes place at their extremities, so that a collar-
the endophyte are not mentioned. In Australia, like structure encircles the entire host root. Two
Diplatia and several other genera are similar in separate vascular cores differentiate within the
this regard (Hamilton and Barlow 1963). It is proximal part of the haustorium as well as two
reported that in the African Agelanthus and lysigenous glandular cavities. Between these two
Moquiniella such bark strands frequently pro- cavities, an extraordinary, U-shaped body of scle-
duce new shoots, as they do in a few Australian renchyma forms that has two pointed, sharp-
species like Amyema congener. Occasionally the edged prongs pointing forwards. The parenchy-
host reaction is vigorous enough to partly bury matous tissue proximal to it appears to push this
the epicortical root. double blade into the host root, where it eventu-
The most extensive endophytic fragmenta- ally severs the host’s stele. Following this, paren-
tion in Loranthaceae occurs in the Chilean mis- chyma invades the space between the severed
tletoe, Tristerix aphyllus, a nearly holoparasitic ends of the host root, and cells from its periphery
species limited to large cacti, and having only invade the nearby host xylem cells by means of
short, leafless inflorescences outside the host. tube-like extensions. It is remarkable to find one
Penetration of the host appears to proceed mostly of the most primitive members of the family
from filamentous invasion via the host’s stomatal having evolved the most sophisticated and elabo-
cavities, the filaments rapidly spreading through- rate endophyte in Santalales.
out host tissues (Mauseth et al. 1985). The con- However, the instances reported above repre-
nection to the external parts of the seedling (the sent highly derived and exceptional conditions. It
connate cotyledons remaining in the endosperm) is regrettable that the anatomical structure of
quickly disintegrates, so that the initial parasitic loranthaceous haustoria, especially the architec-
phase is exclusively endophytic, completely par- ture of the host-parasite interface, has received no
allel to the events in Arceuthobium (Viscaceae). attention in the great majority of genera. It is only
It is not certain whether, in the more standard in the most unusual loranthaceous species, that
“Santalalean” invasion that may also take place we have details available for their admittedly
and in which the usual collapsed zones and cen- exceptional development. Intriguing as these
tral intrusive organ play a part, a glandular area is cases are, they throw little light on the haustoria
differentiated prior to invasion. The uniseriate of most Loranthaceae. The vast majority of Lor-
endophytic filaments eventually become multi- anthaceae are attached to the host mainly by a
seriate, differentiating both phloem and xylem. more or less unified, massive primary haustorium
There is nothing resembling the sinkers of Visca- from which no new shoots arise (even though this
ceae. The precise nature of any connection to the does take place endogenously from the external
host’s vascular strands has not been adequately base of the plant in some cases, as in Phthirusa
delineated. Callus-like nodules develop below the hutchisonii). The host almost invariably responds
host surface, mostly just above its areoles, from by laying down massive tissues embracing, but
which the inflorescences emerge. The part of the not embedding the haustorial organ. In extreme
host so invaded (and floriferous) can be 2–3 m cases this results in the formation by the host of
long. Other species of Tristerix appear to have a the well known, radially grooved, “rosas de palo”
84 Loranthaceae
that may be 40–50 cm in diameter in Psitta- E V O L U T I O N . Diversification and aerial parasit-

canthus, and may be compared to a placenta. ism is believed to have evolved 28–40 m.y.a.
The development of such structures has been (Vidal-Russell and Nickrent 2007, 2008), the lat-
explained by Kuijt and Lye (2005b), and their ter perhaps more than once.
variability in Africa has been charted by Calvin
and Wilson (1998). The secondary haustoria pro- C H R O M O S O M E N U M B E R S . The primary base
duced on epicortical or secondary roots may chromosome number in Loranthaceae is n ¼ 12,
result in smaller but similar structures, but have the other recorded numbers (11, 10, 9, and 8)
not been anatomically described except in the believed to be the result of progressive aneuploid
above-mentioned Ileostylus, Nuytsia, and Atkin- reduction, these reduced numbers corresponding
sonia (Fineran and Hocking 1983), the last two to separate lineages (Nickrent et al. 2010). The
genera not having primary haustoria. size of chromosomes in, for example, Psitta-
As mentioned above, D. Thoday produced a canthus is sometimes equal to, or greater than,
long series of papers about the gross structure of that of any in the plant kingdom, the smallest
the mistletoe endophyte (including Viscaceae), ones being found in the primitive genera Atkin-
but his studies are difficult to summarize or sonia and Gaiadendron (Barlow and Wiens 1971).
place in taxonomic context (see Thoday 1961, Polyploidy is exceedingly rare in the family, tetra-
and his surveys in 1956a, 1956b, 1958). ploids having been demonstrated in Spraguea-
Epicortical roots, in most cases formed from nella, and in at least some individuals of
the base of the plant, are found in numerous Passovia pyrifolia and Gaiadendron punctatum.
genera of Loranthaceae, and always bear second- The n ¼ 16–18 for Desmaria mutabilis requires
ary haustoria. In some cases, these roots may be confirmation.
several meters long, as in Peristethium leptosta-
chyum (Kuijt 2012), each bearing numerous P O L L I N A T I O N . The great majority of Old World
haustoria. In an unexplained fashion, epicortical genera are obligately bird-pollinated and show
roots almost invariably follow the length direc- some remarkable adaptations to this type of pol-
tion of the host branch, primarily in a proximal lination, including the color patterns and floral
direction. In a small number of instances, mostly shapes and positions usually associated with
in neotropical genera, epicortical roots with sec- ornithophily. In a number of genera, fenestrae
ondary haustoria are also formed from shoots, developed in the mature bud allow avian pollina-
often near or on potential host stems. This is tors to insert the bill and physically open the
especially characteristic of Struthanthus and flower. This opening may be explosive, showering
some Peristethium and Passovia species. The the bird with pollen (Kirkup 1998). Frequently,
most dramatic instance is seen in Tripodanthus the style and stigma bend towards the bird imme-
acutifolius, where profuse root formation may diately the flower is opened. There exist two pat-
follow injury or contact with other organs. Such terns among explosive flowers in African
roots may reach the soil and even establish haus- Loranthaceae. The first type involves fenestrae
toria on subterranean host organs. Curiously, the between adjacent corolla lobes below the tip of
related Tripodanthus flagellaris produces two the bud. When the bird’s bill probes such fenes-
slender epicortical roots at most nodes, these trae, the petals above (and sometimes below)
roots perhaps also functioning as tendrils. Shoots separate immediately and the stamens coil
are generated from epicortical roots of some spe- inwardly, with an explosive release of pollen.
cies, notably in Notanthera and Desmaria, where The second pattern is a two-step mechanism
this growth habit allows for a certain amount of that does not involve corolla fenestrae, the flow-
mobility through the host crown as the latter ers being characterized by swollen apices that are
expands. Since some seeds germinate on host tapped or squeezed by the pollinating bird. This
leaves, the early development of epicortical allows the petal lobes to reflex and show the so-
roots growing in a proximal direction can some- called secondary fenestrae between the lower
times save the parasite when a secondary hausto- parts of the filaments. When the bird inserts its
rium is established on a nearby host stem before bill into such secondary fenestrae, individual
the supporting leaf drops. filaments separate and coil inwards, violently
Loranthaceae 85
shedding pollen. In some cases, as in Erianthe- Pollen grains of Loranthaceae tend to be tri-
mum, stamens actually break off, scattering pol- angular in outline, the sides ranging from con-
len in all directions, or entire anthers are shot off cave to convex. Rarely, essentially spheroidal
in the direction of the pollinator. Polhill and shapes are reported, as in Atkinsonia, Phthirusa
Wiens (1998) report that some species of Tapi- hutchisonii, and Tupeia antarctica. While trian-
nanthus secrete nectar at the petal sutures when gular pollen is 3-aperturate, the spheroidal type
the flower is mature to induce avian pollinators to may be 4- or 5-aperturate; Atkinsonia appears to
peck at it, releasing a targeted spray of pollen lack apertures altogether, and is very irregular in
from the anthers. There is no known equivalent shape. Most pollen is syncolpate, but colpi may be
of any such events in the Neotropics, even though distinct or absent at the equator. Margins of the
simple fenestrae have been shown to exist in at colpi may be thickened and psilate in contrast to
least one species of Tristerix (Kuijt 1988). the equatorial surface features between the lobes.
In the New World, very few detailed observa- Heteropolar pollen is rare but known from the
tions have been published on the pollination of African genus Plicosepalus. Ornamentation gen-
the several genera that may justifiably be called erally is psilate, scabrate, verrucate or rarely echi-
bird-pollinated (Aetanthus, Desmaria, Gaiaden- nate, the latter strikingly displayed by Phthirusa
dron, Ligaria, Psittacanthus, Tristerix, and one hutchisonii, in contrast to its congeners. Oryc-
species of Tripodanthus, T. belmirensis). In great tanthus shows three circular depressions on
contrast to many Old World genera, flowers are each face, this being a reliable diagnostic charac-
nearly always actinomorphic. Hummingbirds are ter for the genus. Tripodanthus acutifolius is
the predominant visitors of these genera. In at unusual in having equatorial regions with densely
least one, possibly two, species of Psittacanthus, clustered blunt-tipped spinules strongly contrast-
bat pollination is strongly suspected (Kuijt ing with double, psilate ridges terminating in
2009a). Nothing is known concerning the (prob- expanded equatorial portions. Small-flowered
ably insect-mediated) pollination of the numer- neotropical species generally are oblate, the amb
ous genera and species of small-flowered ranging from trilobate, deeply concave to circu-
neotropical Loranthaceae. This is unfortunate, lar, only a few species being heteropolar. Psitta-
as a recent exploration of anther diversity in two cantus is exceptionally variable in several
genera (Dendropemon and Passovia) indicates palynological features (Feuer and Kuijt 1979).
very specialized conditions (Kuijt 2011a, 2011b). The endexine in the family tends to be greatly
It must be remembered that non-avian pollina- reduced (Lobreau-Callen 1982).
tors may compete with birds in large-flowered
species; I have observed this sort of active com- E C O N O M I C I M P O R T A N C E . Mistletoes, being par-
petition between hummingbirds and butterflies asitic, inevitably withdraw materials from their
around Psittacanthus as well as Gaiadendron in hosts, but the precise extent of that damage is
Costa Rica. In the Australian Nuytsia, also, both essentially impossible to establish with any
insects and birds commonly visit the flowers degree of accuracy, as it depends on the size,
(Watson 2011). The remaining taxa with larger vigor, and age of both partners, along with other
white or colorful flowers in South America seem environmental factors. Observational and anec-
to lack published observations on pollination dotal commentary of this sort, often backed up by
(Notanthera, and two species of Tripodanthus). detailed surveys, abounds especially in the North
American forestry literature on Arceuthobium
P O L L E N M O R P H O L O G Y . It is only in the New (Viscaceae), but defies summary and has no
World that detailed SEM and TEM studies of equivalent in the present family. There can be
loranthaceous pollen have been carried out little doubt, nevertheless, that the long-range
(Feuer and Kuijt 1979, 1980, 1985), although damage to trees can be very significant. In other
some Australian relatives were included. Also, genera of mistletoes, damage to the host has also
the monotypic New Zealand genus Tupeia was been commented on; the reader is referred to
accounted for in an earlier study of Eremolepida- Kuijt (1969, pp. 201–202) for brief details. Tris-
ceae (Feuer and Kuijt 1978). terix corymbosus in southern Chile, several
86 Loranthaceae
Loranthaceae on teak in southwest Asia, and Vis- even desert regions in Africa, Australia, coastal
cum album in certain European countries are Peru and Chile, and north-western Mexico. Host
important in this respect. However, in many trop- species are largely woody dicotyledons, both gym-
ical commercial plantations of cacao, for exam- nosperms and especially monocotyledons being
ple, the parasites are essentially ignored and their largely avoided. Host preferences are uneven or,
effects undiagnosed; I recall counting five differ- in the majority of cases, unknown or uncertain,
ent species of vigorous mistletoes involving three but local preference may be striking, especially in
genera on a single cacao tree in Costa Rica. For a Australia. An exception may be seen in Tristerix
more general summary of economic losses caused aphyllus that is limited to Cactaceae. Certain spe-
by mistletoes, the reader is referred to Gill and cies have adapted to urban environments, as some
Hawksworth (1961). species of Struthanthus in Central America and
In contrast, recent years have seen an Tripodanthus acutifolius in southern Brazil that
emerging appreciation of the integrated role mis- may parasitize ornamental and street trees; others
tletoes play in ecological communities. This is not constitute important pests in plantations of cacao,
surprising when considering the obvious coevo- Hevea brasiliensis, and many others.
lution, for example, of large-flowered neotropical
Loranthaceae with hummingbirds. Additionally, H Y P E R P A R A S I T I S M . In contrast to Viscaceae,
fruit production by mistletoes can be profuse, hyperparasitism on other mistletoes is exceed-
and must constitute a significant source of nutri- ingly rare in Loranthaceae, but Amyema miracu-
ents (and, in xeric environments, of water). losa frequently parasitizes A. miquelii in
No Loranthaceae have the medicinal and Australia (Watson 2011).
historical status of Viscum album but, perhaps
sometimes in extrapolation from that species, P A L E O B O T A N Y . The fossil record of mistletoes
some Loranthaceae are used here and there for a is extremely sparse, which is understandable in
variety of medicinal purposes as, for example, in view of their parasitism in the crowns of trees and
parts of tropical Africa (Burkhill 1995). their frequent ornithophilous pollination system.
For the Cretaceous and early Tertiary of the
H Y B R I D I Z A T I O N . Two documented cases of North American area, the palynological record
hybridization are known for Loranthaceae. The has recently been reviewed by Taylor (1990) but,
first is in Amyema pendulum and A. quandang notwithstanding the studies of contemporary
(Bernhardt and Calder 1981). Secondly, Mueller- pollen by Feuer and Kuijt (1979, 1980, 1985),
ina eucalyptoides x M. celastroides hybrids are continues to be somewhat marred by ambiva-
recorded in coastal New South Wales (Watson lence in the taxonomic position of Gothanipollis.
2011, p. 94). The report on hybridization between The singular exception to this uncertainty seems
Tupeia antarctica and Ileostylus micranthus was to be in Gothanipollis cockfieldensis (Taylor
erroneously based on the variation in sexual 1989). This species has pollen that is strikingly
expression in the former (Nickrent et al. 2010). similar to that of the extant Tripodanthus acuti-
folius, including the apomorphy of baculate-
A F F I N I T I E S . The family is usually thought to be pilate exine elements. As mentioned earlier, the
related especially to Olacaceae. published record of Aetanthus from the Oligo-
Transcontinental affinities are poorly under- cene of Puerto Rico (Graham and Jarzen 1969)
stood except for the primitive trio of genera, is in need of reevaluation, partly because it was
Atkinsonia, Gaiadendron, and Nuytsia that rep- published before the above Feuer and Kuijt work,
resent a Gondwanaland connection. and partly because the assignment of that pollen
to Aetanthus is very unlikely, the genus being a
D I S T R I B U T I O N A N D H A B I T A T S . Loranthaceae small one of the high northern Andes (Kuijt
are predominantly tropical in distribution, very 2014a) the pollen of which is often not distin-
few species being found in colder climates. guishable from that of the far larger and palyno-
Among the latter are Tristerix corymbosus in logically diverse genus Psittacanthus. See also the
southern Chile and Loranthus europaeus in up-to-date summary of fossil pollen by Van der
central Europe. Many species inhabit drier or Ham in Barlow (1997).
KEY TO THE GENERA OF LORANTHACEAE OF THE NEW WORLD 87
C O N S E R V A T I O N . The importation of opossums 2. Petals bright yellow, nearly 40 cm long, turning

in New Zealand has had negative effects on Lor- orange in age; short-shoots present, bearing the flow-
anthaceae, as they constitute a favorite food item. ers at the tip; plants deciduous 4. Desmaria
Tupeia antarctica is thus locally protected by – Petals white and pink, to 12 mm long; short-shoots
lacking; plants evergreen 8. Notanthera
means of metal cladding beneath the mistletoe.
3. Petals <12 mm long, often greenish white or reddish,
not bright yellow 4
SUBDIVISION AND RELATIONSHIPS WITHIN THE – Petals mostly >12 mm long, mostly brightly colored,
F A M I L Y . A recent, comprehensive study of the including yellow or white 14
family, largely based on molecular analysis and 4. Flowers sessile in leaf axils, tetramerous; inflores-
within the context of the Santalales (Nickrent et al. cences lacking 14. Phthirusa
2010), has suggested the following organization: – Flowers in axillary and/or in terminal inflorescences;
petals 4, 5, or 6 5
Tribe Nuytsieae Tiegh. (W Australia: Nuytsia floribunda).
5. Inflorescences mostly determinate, subtended by
Tribe Gaiadendreae Tiegh. (E Australia: Atkinsonia ligus- chartaceous, partly caducous leaf scales
trina; Andean America, mostly: Gaiadendron punctatum, 13. Peristethium
G. grahami; Bolivia to Nicaragua and Venezuela).
Tribe Elytrantheaea Engler (Australia, New Zealand, – Inflorescences determinate or indeterminate, lacking
Asia, W Pacific: 14 genera). basal caducous leaf scales 6
Tribe Psittacantheae Horan. (a subtribe by Engler; New 6. Inflorescences monadic only 7
World; 1 species in New Zealand). – Inflorescences triadic or dyadic only (one or 2 excep-
Subtribe Tupeiinae (“Tupeinae”: sic) Nickr. and Vidal-R. tions, Mexico and Bolivia) 12
(New Zealand: Tupeia antarctica). 7. Monads ebracteolate; inflorescences mostly determi-
Subtribe Notantherinae Nickr. and Vidal-R. (S Chile: Des- nate 2. Cladocolea
maria and Notanthera). – Monads bracteolate, the bracteoles separate or con-
Subtribe Ligariinae (“Ligarinae”) Nickr. and Vidal-R. nate with the bract; inflorescence mostly indetermi-
(Ligaria and Tristerix). nate 8
Subtribe Psittacanthinae Engl. (ca. 12 genera, tropical 8. Bracteoles and bracts connate into a cupule; monads
America). pedicellate or sessile 9
Tribe Lorantheae Rchb. (Old World only; 40 genera). – Bracteoles distinct, small; flowers sessile 1 0
Subtribe Ileostylinae Nickr. & Vidal-R. (New Zealand, 9. Staminodia and fertile stamens alternating; anthers
Ileostylus; E Australia, Muellerina). basifixed or nearly so; Caribbean only
Subtribe Loranthinae Engler (SW Pacific, Cecarria; and 3. Dendropemon
Europe to S China and Sumatra, Loranthus). – All stamens fertile; anthers dorsifixed, versatile;
Subtribe Amyeminae Nickr. and Vidal-R. (Australia, SE Chiriquı́ only 11. Panamanthus
Asia, W Pacific: 9 genera). 10. Bracteoles narrow, strap-like; pollen with 3 circular
Subtribe Scurrulinae Nickr. and Vidal-R. (China, SE Asia, depressions on each face; leaf mesophyll with stellate
Scurrula; Tropical Asia and coastal E Africa, Taxillus). fiber bundles 9. Oryctanthus
Subtribe Dendrophthoinae Nickr. and Vidal-R. (tropical – Bracteoles naviculate, not strap-like, or minute;
Africa to SW Asia and Australia). pollen lacking circular depressions; leaf mesophyll
Subtribe Emelianthinae Nickr. and Vidal-R. (Africa and lacking stellate fiber bundles 11
Arabia; 7 genera). 11. Bracteoles naviculate, prominent; stamens with fila-
Subtribe Tapinanthinae Nickr. and Vidal-R. (Africa, ments and evident connectival prominence; northern
Arabia, Madagascar; 14 genera). Venezuela, Colombia, and Costa Rica (Osa Peninsula)
7. Maracanthus
KEY TO THE GENERA OF LORANTHACEAE – Bracteoles extremely small, neither naviculate nor
OF THE NEW WORLD strap-like; anthers sessile, minute; eastern Brazil
(one species in Guyana) 10. Oryctina
12. Inflorescence a capitulum with 2(4) triads; flowers
See also Kuijt, Blumea 27: 1–73 (1981). tetramerous, usually bisexual; young parts tomentose;
epicortical roots present or not
1. Epicortical roots on host branches generating leafy 16. Pusillanthus
shoots; endemic to southern Chile 2 – Inflorescence racemic or spike-like, not a capitulum;
– Epicortical roots not, or only very rarely, generating surfaces glabrous or partly furfuraceous (tomentose
leafy shoots, or epicortical roots absent, plants some- in one Bolivian species of Struthanthus); epicortical
times (Gaiadendron) terrestrial shrubs; not present in roots mostly present
Chile except Ligaria 3 13
88 Loranthaceae
13. Anthers basifixed or nearly so, often “Passovian”;

flowers bisexual or plants dioecious
12. Passovia
– Anthers elongate, versatile, filaments slender (very
rarely absent); plants dioecious
17. Struthanthus
14. Flowers in triads or dyads 15
– Inflorescence bearing monads, or inflorescences
absent 18
15. Floral bracts and bracteoles foliaceous; primary haus-
torium lacking; shrubs or small trees, terrestrial or on
tree branches 5. Gaiadendron
– Floral bracts and bracteoles not foliaceous (except for
the bracts of some Tristerix); primary haustorium
present; branch-parasitic on shrubs or trees 16
16. Seeds with endosperm; epicortical roots from base of
plants and/or from the stem (uncertain in T. belmir-
ensis); inflorescence triadic
18. Tripodanthus
– Seeds lacking endosperm; epicortical roots mostly
lacking; inflorescence triadic or dyadic
17
17. Anthers needle-like, as thin as the filament, basifixed,
with acicular tip; inflorescence dyadic; flowers mostly
pendent; higher Andes
1. Aetanthus
– Anthers not needle-like, thicker than the
filament, mostly dorsifixed, lacking acicular tip
(exception: P. hamulifer); inflorescence triadic or
dyadic, flowers pendent or not; lower and middle
elevations, Mexico to Bolivia and Argentina Fig. 15. Loranthaceae. Aetanthus nodosus. A Flowering
15. Psittacanthus plant. B Anther. C Mature fruit. (Kuijt 1986, drawn by
18. Inflorescence a raceme; cotyledons initially cryptoco- author)
tylar, connate apically; leaves with apical sclerotic nail
only in T. chodatianus
19. Tristerix whorled. Inflorescences in foliar axils or
– Inflorescence lacking, flowers individually attached, produced endogenously from nearby nodal
axillary in position, pedicellate; cotyledons spreading areas, being umbels bearing 2–4 dyads. Flowers
following establishment; leaves with apical sclerotic
nail except in L. teretiflora 6. Ligaria pedicellate, mostly pendant, long and slender,
usually brilliantly red with golden yellow tip, the
buds with acute apex; petals and stamens 6,
GENERA OF LORANTHACEAE OF THE NEW stamens usually clustered at the center against
WORLD the style, nearly isomorphic; anther basifixed,
of the same thickness as the filament and difficult
to distinguish from it, with attenuate, needle-
1. Aetanthus (Eichler) Engler Fig. 15
like apex; pollen sacs extremely long and
Aetanthus (Eichler) Engler, Nat. Pflanzenfam. III, 1: 189 slender; style slender, reaching beyond the
(1889); Kuijt, Pl. Div. Evol. (2014a), rev. anthers, stigma weakly differentiated. Fruit a
Psittacanthus subgen. Aetanthus Eichler (1868). large berry. Seed lacking endosperm; embryo
massive and consisting mostly of 2 fleshy, flat
Robust, glabrous plants with single, large cotyledons, haustorial pole weakly differentiated
haustorial attachment, epicortical roots lacking; at maturity. n ¼ 8.
branching percurrent, or di-/trichotomous and A genus of 15 spp., closely related to Psitta-
determinate with innovations of a single inter- canthus but sharply distinct from it by its needle-
node aborting terminally. Leaves decussate or like, exceedingly long and slender, basifixed
GENERA OF LORANTHACEAE OF THE NEW WORLD 89
anthers with acicular tips, and by its consistently

dyadic inflorescence, the flowers mostly pendant.
Aetanthus ranges from northern Colombia and
adjacent Venezuela to northern Peru, and is lim-
ited to high elevations.
2. Cladocolea Tiegh. Fig. 16
Cladocolea Tiegh., Bull. Soc. Bot. France 42: 166–168

(1895); Kuijt, J. Arnold Arb. 56: 265–335 (1975); Kuijt,
Novon 2: 351–354 (1992), rev.
Phthirusa Mart. (1830), p.p.
Plants of moderate size, glabrous to short-pubes-

cent; epicortical roots from the base and/or
stems present in some species, absent in others.
Leaves decussate, alternate or irregularly placed,
rarely reduced to scales in part. Inflorescence
commonly a determinate spike, capitulum, or
raceme, rarely a dichasium. Flowers bisexual
or plants dioecious, lacking bracteoles, sessile
or pedicellate, 4-, 5-, or 6-partite; stamens epipe-
talous in two series or at equal heights; style
(Mexico) sometimes greatly contorted or genicu-
late, especially in staminate flowers. Fruit a
one-seeded berry with endosperm; embryo
dicotylous. n ¼ 8.
A genus of some 25 spp., mostly concen-
trated in Mexico but with some species further
south, including Andean Ecuador and adjacent Fig. 16. Loranthaceae. Cladocolea harlingii. A Flowering
Peru. plant (note grasping petioles, arrow, and epicortical stem
roots). B Inflorescence. C Floral details. D Fruit. (Kuijt
1975, drawn by author)
3. Dendropemon (Blume) Reichenb.
Dendropemon (Blume) Reichenb., Rept. Herb.: 73 (1841);

Kuijt, Syst. Bot. Monogr. 92: 1–110 (2011), rev. connate with the pedicel and two bracteoles,
Loranthus sect. Dendropemon Blume (1830). together forming a more or less united cupule
Phthirusa sect. Dendropemon (Blume) Eichler (1868). subtending a single flower. Flowers hexamerous,
bisexual, petals slightly dimorphic, yellow to
Leafy mistletoes of moderate size; internodes reddish, calyculus inconspicuous, bud apex
terete to quadrangular, glabrous or with furfurac- acute to rounded; stamens of two series, the
eous surface; epicortical roots present in many, longer ones sterile or non-functional, often
possibly all, spp., mostly from the base; vegetative white or prominently colored, their flat filaments
reproduction rare. Leaves paired, smooth-mar- with lateral cavities accommodating the pollen
gined, linear to (ob)ovate or lanceolate, apex, sacs of adjacent, shorter, fertile stamens, anthers
base and petiole various, venation pinnate. dorsifixed (seemingly basifixed); shorter stamens
Inflorescences axillary and simple (very rarely sometimes with small connectival horns; style
compound), mostly solitary, spicate, racemose, straight, stigma capitate. Fruit a one-seeded
or umbellate, with various numbers of paired berry, variously colored, often bicolored and
monads. Monads each with the primary bract banded, (ob)ovoid to ellipsoid. Seeds with
90 Loranthaceae
copious, whitish endosperm; viscin developed

especially at the radicular pole; embryo bicotylar,
bright green, with expanded, rounded haustorial
pole. n ¼ 8.
32 spp., endemic to Caribbean islands and
Bahamas.
4. Desmaria Tiegh.
Desmaria Tiegh., Bull. Soc. Bot. France 42: 458–459

(1895); Kuijt, Pl. Syst. Evol. 151: 121–130 (1985), rev.
Phrygilanthus Eichler (1868), p.p.
Large mistletoes with long epicortical roots

sprouting new shoots, exhibiting shoot dimor-
phism: short shoots lateral on older long shoots
and bearing 6–10 leaves and, eventually, an
umbel-like terminal raceme of 4–10 triads; triads
with blunt bracts and bracteoles, median flower
sessile, lateral ones on pedicels 1 mm long. Leaves
decussate or whorled, deciduous, thin; vegetative
shoots with terminal bud scales during the
dormant season. Flowers yellow, becoming red-
dish in age; petals 6, nearly 3.5 cm long, the
distinct limbs standing sideways at anthesis;
filaments and stamens of two different lengths
(10–15 mm), with dorsifixed, versatile, yellow Fig. 17. Loranthaceae. Gaiadendron punctatum. A Flow-
anthers 2 mm long; style slender, nearly as long ering branch. B Postanthetic floral triad. C Flower. D
as the petals, stigma small; ovary 5 mm long, Fruit. (Kuijt 1986, drawn by author)
narrowly cylindrical, including the 1.5 mm long,
membranous, smooth-rimmed calyculus. Fruit a
other epiphytes; branches more or less terete.
one-seeded berry with conspicuous calyculus,
Leaves paired, shiny, lanceolate to ovate, margins
endosperm present; seedling heterocotylar, one
revolute. Inflorescence terminal and/or axillary,
cotyledon peg-like and remaining in the endo-
each a raceme of paired triads; triads short-
sperm, the other expanding to an orbicular,
pedunculate, the median flower sessile and
green foliar organ. n ¼ 16.
subtended by a foliar bract, the lateral ones
One sp., Desmaria mutabilis (Poepp. & Endl.)
short-pedicellate and subtended by smaller foliar
Tiegh. ex Jackson; endemic to southern Chile,
bracteoles. Flowers mostly golden yellow (some-
perhaps exclusively on Nothofagus. Shoot dimor-
times white), petals 7 or fewer, stamens of 2 or 3
phism is also known in some African Lorantha-
lengths, anthers versatile, dorsifixed. Fruit a dull
ceae (Polhill and Wiens 1998) and in
orange or black berry lacking viscin, spherical or
Psittacanthus palmeri.
ellipsoid, calyculus absent (G. punctatum) or
prominently persistent (G. coronatum), endo-
5. Gaiadendron G. Don Fig. 17 sperm white, with longitudinal grooves; embryo
slender, dicotylous, not developing a primary
Gaiadendron G. Don, Gen. Hist. 3: 431–432 (1834). haustorium when germinating; germination
Phrygilanthus Eichler subgen. Taguana (1868). epigeous. n ¼ 12.
G. punctatum Ruı́z & Pavón, a variable sp.,
Shrubs or small trees, stoloniferous, terrestrial or ranging from Nicaragua to Bolivia, with isolated
sometimes epiphytic on trees while parasitizing stations east to Mount Roraima, and a second
rare species from central Peru (G. coronatum stamen series) and dorsifixed, apex of anther with
Kuijt). Gaiadendron, along with the Australian papillate or massive connectival protuberance.
monotypic genera Atkinsonia and Nuytsia, form Style straight; stigma capitate, distinct. Fruit an
the trio of basal genera of Loranthaceae. oblong, one-seeded berry, embryo dicotylous,
cotyledons long and narrow, haustorial pole
6. Ligaria Tiegh. weakly developed.
Three species, two in northern Venezuela,
Ligaria Tiegh., Bull. Soc. Bot. France 42: 345–349 (1895); one in Costa Rica (Osa Peninsula).
Kuijt, Brittonia 42: 66–69 (1990), rev.
8. Notanthera G. Don
Robust, glabrous plants, stems rigid, innovations
determinate, terete, epicortical roots lacking; Notanthera G. Don, Gen. Hist. 3: 428 (1834).
plants with a single haustorial connection. Phyl- Loranthus sect. Notanthera DC. (1830).
lotaxy alternate, leaves cuneate with dark scle-
rotic tooth (L. cuneifolia) or obovate and Densely leafy plants with persistent, papillate
lacking terminal tooth (L. teretifolia). Inflores- hairs on young growth, growing in the crowns
cence lacking, flowers singly or in small clusters and outer limbs of trees, with profuse, slender
at the nodes, pedicellate, brilliantly red; petals epicortical roots regenerating aerial shoots, both
and stamens 6, stamens dimorphic, anthers primary and secondary haustoria large and knob-
versatile, dorsifixed. Fruit dark blue, with promi- like. Internodes terete; leaves shiny, dark green,
nent, funnel-shaped calyculus, seed with endo- irregularly paired to alternate or in whorls of 3.
sperm; seedling dicotylous, with tubercular Inflorescences clustered near shoot ends, one per
surface below the cotyledons; germination cryp- leaf axil as well as a terminal one, each being a
tocotylar. n ¼ 10. dense raceme of numerous, paired triads; triad
Two spp., L. teretiflora (Minas Gerais) and peduncles 4–5 mm long, median flower sessile,
L. cuneifolia (Central Chile, Uruguay, northern lateral flowers on pedicels 2 mm long, bracts and
Argentina, eastern Bolivia to central Peru). bracteoles narrow, acute. Flower bud white, with
bright pink, clavate tip, petals 6, isomorphic;
7. Maracanthus Kuijt stamens white, essentially isomorphic, anthers
dorsifixed, versatile. Fruits purplish becoming
Maracanthus Kuijt, Brittonia 28: 231–238 (1976); Kuijt, black, endosperm copious, light green. Seedlings
Novon 17: 476–478 (2007); Kuijt, Novon (2014b), rev. dicotylous, phanerocotylous. n ¼ 12.
Oryctina Tiegh. (1895), p.p. One sp., Notanthera heterophyllus (Ruiz &
Pavon) G. Don; southern Chile.
Glabrous or partly furfuraceous plants, percur-
rent or determinate by apical abortion, dioecious
or with bisexual flowers; internodes terete and 9. Oryctanthus Eichler Fig. 18
essentially glabrous or quadrangular with con-
spicuous furfuraceous stripes; epicortical roots Oryctanthus Eichler in Mart., Fl. brasil. 5(2): 87–88 (1868);
Kuijt, Bot. Jahrb. Syst. 95: 478–534 (1976); Kuijt, Bot.
unknown or basal (M. costaricensis). Leaves Jahrb. Syst. 114: 173–183 (1992); Kuijt, Novon 21:
paired, oblanceolate to broadly elliptical, apex 463–467 (2011), rev.
rounded, base with or without distinct petiole; Loranthus Jacq. sect. Oryctanthus Eichler subgen. Paryc-
venation pinnate. Inflorescences simple, axillary tanthus Kuijt (1976).
spikes and/or terminal, pedunculate to sessile,
bearing pairs of scale-leaves subtending single, Leafy plants, stems often with furfuraceous cover
sessile flowers; each flower flanked by a pair of at least when young, or striped furfuraceous; epi-
acute, conspicuous, naviculate bracteoles, hex- cortical roots mostly from the base, not from
amerous, petals dimorphic; stamens dimorphic, stems, rarely absent at maturity. Phyllotaxy
attached at two different heights, with 2 or 4 decussate; leaves leathery, with characteristic
pollen sacs, filaments short (or lacking in short stellate fiber bundles along smaller veins.
92 Loranthaceae
dicotylous, with massive cotyledons and promi-

nent haustorial disk. n ¼ 8.
A distinctive genus of 13 spp. ranging from
southern Mexico to Bolivia and northern Brazil,
with one species established on Jamaica.
10. Oryctina Tiegh.
Oryctina Tiegh., Bull. Soc. Bot. France 42: 168–169 (1895);

Kuijt, Pl. Syst. Evol. 137: 215–219 (1981); Kuijt, Novon 10:
391–397 (2000), rev.
Leafy plants of moderate size, at least some

species with basal epicortical roots. Leaves decus-
sate. Inflorescences indeterminate spikes bearing
pairs of minute, sessile flowers (monads), each
flower with small primary bract and two minute
lateral bracteoles. Flowers bisexual or plants
monoecious, 6-merous; petals somewhat dimor-
phic, stamens placed in two series, anthers 2(4)-
loculate, minute, sessile. n ¼ 8.
A genus of 6 spp. primarily of north-central
Brazil but with one sp. in Guyana.
11. Panamanthus Kuijt
Panamanthus Kuijt, Ann. Missouri Bot. Gard. 78: 172–176

(1991).
Scandent plants of Struthanthus-like habit,

sparsely branched, internodes somewhat qua-
drangular when young, soon becoming terete,
Fig. 18. Loranthaceae. Oryctanthus florulentus. A Flow-
ering branch. B Spike. C Floral details. D Pollen grain. with occasional epicortical roots from branches
(Kuijt 1976, drawn by author) and (presumably) from the base. Leaves decus-
sate, ovate, apex contracted into slender tail, base
Inflorescences solitary and axillary where clus- truncate to obtuse. Inflorescences in small, axil-
tered at the nodes, or in compound, terminal, lary clusters, short-pedunculate with some cadu-
squamate arrangement, individually each a cous scale leaves, each a raceme of 6–8 pairs of
spike with often swollen axis, the flowers single, monads; monad peduncle 2–3 mm long, connate
sessile in cavities axillary to leaf scales, where along its length with an acute bract and embrac-
flanked by 2 minute, flat, strap-like bracteoles ing 2 acute bracteoles together forming a cupule
just reaching the rim of the bract. Flowers bisex- clasping the base of the flower. Flowers 8–9 mm
ual, 6-merous (one 4-merous species), yellow to long, bisexual, hexamerous, petals very slightly
dark red; petals and stamens dimorphic, anthers dimorphic; ovary very short (1 mm), bud apex
basifixed, mostly 4-loculate; pollen with 3 charac- acute; anthers dimorphic, 4-loculate, with termi-
teristic, circular depressions on each face; style nal connectival horn, basifixed or nearly so, fila-
straight, with small, capitate stigma. Fruit green- ments extremely short (0.5 mm); style straight,
ish, yellow-green, red to purple, or black; endo- stigma undifferentiated. Fruit nearly 1 cm in
sperm copious, yellowish white; mature embryo diameter, spherical, yellowish orange, with little
viscin tissue. Embryo small, slender, dicotylous,

haustorial pole not expanded.
One sp., Panamanthus panamensis (Rizz.)
Kuijt, endemic to western Panama (Chiriquı́).
12. Passovia Karsten Fig. 19
Passovia Karsten, Bot. Zeit. 4: 107 (1846); Kuijt, Plant Div.

Evol. 129: 159–211 (2011), rev.
Phthirusa sensu Eichler (1868), p.p., not Mart.
Furarium Rizz. (1956).
Phthirusa Mart. sect. Passovia (Karsten) Rizz. (1956).
Leafy, percurrent plants, glabrous or with partly/

entire furfuraceous surface; internodes terete to
keeled; epicortical roots with secondary haustoria
present at the base and, in some (dioecious) spp.,
also on the stems. Leaves decussate, ovate to lance-
olate. Inflorescences mostly axillary, solitary or
with 1 or more additional, superposed and/or pro-
phyllar ones, simple or branched, sometimes ter-
minal, each unit an indeterminate raceme or spike
of paired triads, each triad with at least the median
flower sessile and subtended by one bract and
2 bracteoles showing various degrees of fusion.
Flowers mostly 6-partite, rarely 4-partite, small,
dark red to creamy white, bisexual or plants dioe-
cious; stamens dimorphic, of 2 different lengths,
the longer ones sometimes with bilocular (rarely
non-functional) anthers, others 4-locular; filaments
short and anthers nearly sessile in some species, in
others flat and, in the longer stamens, with conspic-
uous lateral depressions accommodating the
anthers of the shorter series; anther often with
terminal connectival horn; style straight. Fruit a
one-seeded berry, of diverse (sometimes multiple)
colors, seed with copious creamy endosperm, and
viscin. Embryo dicotylous, bright green, fleshy,
with expanded haustorial pole. n ¼ 8. Fig. 19. Loranthaceae. Passovia robusta. A Flowering
A basically continental genus, species num- shoot. B Fruit. C, D Pistillate and staminate floral details,
respectively. (Kuijt 1986, drawn by author)
ber unknown, at least 30; Mexico to Brazil and
Bolivia, with minor representation on Jamaica smooth or with numerous lenticels; epicortical
and Grenada. roots on some branches and basally in at least
some spp., without vegetative reproduction.
13. Peristethium Tiegh. Leaves paired, petiolate, ovate to elliptical, apex
mostly acute to acuminate. Dioecious or flowers
Peristethium Tiegh., Bull. Soc. Bot. France 42: 175 (1895); bisexual. Inflorescences axillary, with basal,
Kuijt, Ann. Missouri Bot. Gard. 98: 542–577 (2011), rev. mostly caducous pairs of leaf scales, monadic,
triadic or mixed, triads below monads, most
Sparsely branched, mostly percurrent plants (1 sp. spp. with a single terminal flower; one sp.
determinate), internodes terete to quadrangular, (P. confertiflorum) with a few pentads among
94 Loranthaceae
triads. Flowers hexamerous or tetramerous

(pentamerous in one sp.); petals slightly dimor-
phic; anthers minute, 4-loculate, basifixed or
essentially sessile, minute, placed just below the
petal tips at 2 different heights or nearly so; style
straight or convoluted in upper portion, appar-
ently absent in staminate flowers of some species,
stigma capitate, often oblique. Fruit a one-seeded
berry. Seed with viscin, endosperm present, at
least sometimes hexangular, embryo dicotylar,
slender, the radicular pole not expanded.
A continental genus of 15 spp., from Amazo-
nian Bolivia and adjacent Brazil through Peru,
Ecuador, Colombia and Venezuela into Panama
and Costa Rica, with two narrow endemics in the
Mt. Roraima-Pakaraima Mountain area.
14. Phthirusa Mart. Fig. 20
Phthirusa Mart., Flora 13: 110–111 (1830); Kuijt, Brittonia

19: 62–67 (1967); Kuijt, Brittonia 46: 72–74 (1994); Kuijt,
Plant Div. Evol. 129: 159–211 (2011), rev.
Ixocactus Rizz. (1952).
Plants of modest size, glabrous; epicortical roots

(even from stems) in some spp., lacking in most;
stems terete or nearly so, or quadrangular, or
internodes flattened into phyllodes (P. hutchiso-
nii). Leaves decussate or irregularly placed,
ovate-(ob)lanceolate to narrowly lanceolate or
partly or entirely scale-like. Dioecious or flowers Fig. 20. Loranthaceae. Phthirusa hutchisonii. A Habit.
bisexual. Inflorescences lacking, the flowers ses- B Flower bud. C Same, two petals removed. D Two petals
with stamens. E Fruit. (Kuijt 1986)
sile, small, placed in leaf axils or clustered on
older, leafless nodes, 4-merous; anthers minute,
2- or 4-loculate, isomorphic or nearly so; style Mostly rather large plants, glabrous, rarely short-
stout, basally expanded in some species, stigma pubescent or furfuraceous, epicortical roots very
capitate. Fruit a small, one-seeded berry. n ¼ 8. rarely present, the primary haustorium becoming
A genus of 7 spp., two in eastern Brazil, 3 in very large (25 cm in diameter or more) in some
the northern Andes, and 2 in West-Central Mex- spp. Stems variously shaped, in some spp.
ico. The genus was greatly altered by Eichler aborting terminally after forming 1 or more leaf-
(1868), most of the species added then and sub- bearing nodes. Leaves decussate, alternate, or
sequently being placed in Passovia. whorled, lacking in P. nudus. Inflorescences basi-
cally a raceme of dyads or triads, rarely reduced
to a capitulum (P. palmeri, Mexico) or to a pair of
15. Psittacanthus Mart. Figs. 3, 21 dyads; inflorescences terminal or lateral, or both,
in several spp. originating endogenously from the
Psittacanthus Mart., Flora 13: 106–107 (1830); Kuijt, Syst. nodes. Flowers hexamerous, pendulous or not,
Bot. Monogr. 86:1–361 (2009), rev. mostly brightly colored in red or red and yellow,
Loranthus Jacq. sect. Psittacanthus (Mart.) Benth. (1880). stamens in one or two different series, mostly
Psathyranthus Ule (1906 [1907]). with long, slender filaments attached dorsally to
terete, young ones short-tomentose, older ones

densely covered with small, pustule-like lenticels.
Leaves small, thin, narrowly oblanceolate, with 3
(5) prominent basal veins; petiole 1 mm, base
acute, apex rounded. Inflorescences solitary, axil-
lary, peduncle extremely slender; flowers 6 (12),
in 2 (rarely 4) sessile triads forming a terminal
capitulum; bracts and bracteoles minute. Flowers
bisexual (rarely pistillate), tetramerous; bud
1.5 mm long; petals isomorphic; stamens isomor-
phic, filaments 0.5 mm long, basifixed; anthers
apparently bilocular, with short connectival
horn; style straight, stout, stigma capitate, papil-
late. Fruit ellipsoid, yellow with red base, calycu-
lus evident.
One sp., P. pubescens (Rizz.) Caires, in north-
ern Venezuela, Guyana, and eastern Brazil (Bahia
to Paraı́ba).
17. Struthanthus Mart. Fig. 22
Struthanthus Mart., Flora 13: 102–106 (1830), nom. gen.

cons. # 2078; Kuijt, Bot. J. Linn. Soc. 142: 469–474 (2003),
rev.
Spirostylis Presl in Schult. & Schult. f. (1829).
Loranthus Jacq. [unranked] Struthanthus a. Struthanthus
(Mart.) Benth. (1880).
Fig. 21. Loranthaceae. Psittacanthus pangui. A Flowering
branch. B Dissected tip of bud. C Dissected base of bud. Scandent, leafy, glabrous plants; internodes terete
D Mature fruit. (Kuijt 1986, drawn by author)
to quadrangular; epicortical roots both from the
base and from the stems. Leaves paired, variously
the anther in a versatile fashion; pollen sacs 4, shaped. Dioecious, with aborted organs of the
sometimes long and divided into numerous min- opposite sex present. Inflorescences mostly axil-
ute loculi and often with a distinctive connectival lary, indeterminate, and simple, one to several
tip, with long, reddish, shiny hairs in the anther per axil, each a raceme or spike of 2–many pairs
region in some species; style nearly as long as the of triads, very rarely (Mexico, and one sp. in
petals, with small, capitate stigma. Fruit a large, Ecuador-Peru) with subterminal monads and a
mostly blackish berry. Seed lacking endosperm, terminal flower; triads pedunculate or sessile,
the cotyledons massive, 2–12 per embryo. n ¼ 8. the median flower mostly sessile, the lateral ones
A genus of at least 120 species, ranging from short-pedicellate; bracts and bracteoles persistent
Baja California to Bolivia and northern Argen- or deciduous. Flowers 6-merous (4- or 5-merous
tina, with a small representation on Jamaica and in S. salicifolia), greenish white; stamens usually
the Lesser Antilles. with prominent, slender filaments; anthers dorsi-
fixed, versatile; style straight in most species,
16. Pusillanthus Kuijt convoluted in a few Mexican ones. Fruit a 1-
seeded berry. Endosperm and viscin copious;
Pusillanthus Kuijt, Novon 18: 370–373 (2008); Caires, embryo dicotylous, bright green, fleshy, with
Gomes-Bezerra & Barnes Proença, Acta Bot. Brasil. 26: expanded haustorial pole. n ¼ 8.
668–674 (2012), rev. A strictly continental, perhaps polyphyletic
genus with an uncertain number (ca. 45) of spp.,
Delicate plants; host attachment saddle-like; epi- ranging from NW Mexico to Bolivia and Argen-
cortical roots lacking (rarely present); internodes tina.
96 Loranthaceae
Fig. 22. Loranthaceae. Struthanthus orbicularis. A Plant Fig. 23. Loranthaceae. Tripodanthus acutifolius. A Flow-
with young inflorescence. B, C Staminate and pistillate ering plant. B Inflorescence triad shortly after flowering.
flowers, respectively. D Young twig with prehensile leaves. C Mature fruit. (Kuijt 1986, drawn by author)
E Mature fruits. (Kuijt 1964b, drawn by author)
or (T. belmirensis) red, hexamerous; stamens of
two different series but anthers isomorphic, dor-
18. Tripodanthus (Eichler) Tiegh. Fig. 23 sifixed, versatile; style slender, straight, stigma
small, capitate. Fruit a 1-seeded berry. Endo-
Tripodanthus (Eichler) Tiegh., Bull. Soc. Bot. France 42: sperm present; embryo slender, bicotylar, haus-
178 (1895); Roldán & Kuijt, Novon 15: 207–209 (2005), torial pole not expanded. n ¼ 8.
rev.
Phrygilanthus Eichler subgen. Tripodanthus Eichler Three spp., T. acutifolius, from Paraguay
(1868). through (infrequently) Andean Peru and Ecua-
dor, and in southern Brazil; T. flagellaris in north-
Glabrous, percurrent plants; internodes terete to ern Argentina, Uruguay, and southern Brazil; and
somewhat quadrangular; epicortical roots pro- the rare, red-flowered T. belmirensis Rold. & Kuijt
duced on stems at least in two species, profusely in Colombia (Antioquia).
so in T. acutifolius (Ruı́z & Pavón) Tiegh., and
two flanking each petiole in T. flagellaris (Cham. 19. Tristerix Mart. Fig. 24
& Schlecht.) Tiegh., but perhaps none in
T. belmirensis Rold. & Kuijt. Leaves decussate or Tristerix Mart., Flora 13: 108–109 (1830); Kuijt, Syst. Bot.
alternate, ovate or linear, venation pinnate. Inflo- Monogr. 19: 1–61 (1988), rev.
rescence a raceme of pedunculate triads, all three Phrygilanthus Eichler subgen. Quintralia Eichler (1868).
flowers of each triad pedicellate, bracteoles and Loranthus Jacq. sect. Phrygilanthus subsect. Metastachys
bracts deciduous or not. Flowers bisexual, white Benth. (1880).
KEY TO THE GENERA OF LORANTHACEAE OF AFRICA AND MADAGASCAR 97
KEY TO THE GENERA OF LORANTHACEAE

OF AFRICA AND MADAGASCAR
1. Madagascar and nearby islands 2

– Continental Africa (adapted from Polhill and Wiens
1998) 3
2. Plants glabrous, including the inner surface of petals;
filaments very short, erect at anthesis
3. Bakerella
– Plants (at least when young) with multicellular/
branched hairs; inner, distal petal and stylar surface
with short simple hairs; filaments distinct, recurved at
anthesis 19. Socratina
3. Hairs simple, irregularly branched or lacking 4
– Hairs stellate or dendritic with whorls of branches,
rarely present only on youngest parts, sometimes
with subsimple hairs admixed 17
4. Inflorescence a raceme or spike, sometimes crowded
at apex of peduncle; petals four, separate, coherent
below, radially spreading to reflexed from the middle
where the short erect stamens are generally attached
(higher in H. periclymenoides) 9. Helixanthera
– Inflorescence capitulate, umbellate, in clusters or sin-
gle; petals not as above (see also Oedina pendens,
Fig. 24. Loranthaceae. Tristerix longebracteatus. A Flow- having dendritic hairs only on the youngest parts,
ering branchlet. B Anthetic flower. C Fruits. (Kuijt 1986, but with racemes bearing large, long-tubed, red flow-
drawn by author) ers) 5
5. Corolla ca. sigmoid, elongate, with marked folds on
the inner surface of the lower part of the petals or
Glabrous or nearly so; branching sympodial, one corolla tube; extensive epicortical roots present bear-
sp. (T. aphyllus) leafless and inflorescences arising secondary haustoria 17. Plicospepalus
ing directly from the endophyte, elsewhere with – Corolla gamopetalous with a short to long tube
single attachment, possibly also sprouting from lacking internal folds; epicortical roots absent 6
endophytic strands in T. corymbosus; epicortical 6. Corolla open, with radially arranged lobes spreading
roots absent. Phyllotaxy alternate, paired, that later reflex, tubular below 7
or whorled in threes; leaf blade simple, ovate- – Corolla opening laterally, often with a marked V-slit,
sometimes (Oncocalyx, Spragueanella) the lobes only
cordate to cuneate. Inflorescence terminal, race- slightly coherent to one side (at least when seen
mose or spike-like, sometimes with smaller, pressed), but then short tube deeply split 9
lateral ones nearby; each flower subtended by a 7. Petals 4; stamens remaining attached to the style-tip
foliaceous or small bract or (in two Chilean spp.) by connective appendages 5. Emelianthe
additionally with 2 acute bracteoles. Flowers acti- – Petals 5, stamens erect to spreading, separate 8
nomorphic, brilliant red or red with golden yel- 8. Filaments curving gently outwards, essentially isodia-
low, one sp. bright pink, 4- or 5-merous, floral metric, attached near base of corolla lobes
elements isomorphic or nearly so, the epipetalous 15. Pedistylis
stamens with long, slender filaments and large, – Filaments erect, upper part thickened and coiling at
anthesis, attached nearly halfway up corolla lobes
versatile, dorsifixed anthers; style about as long as 1. Actinanthella
petals, stigma capitate but small; calyculus nearly 9. Corolla lobes inrolled at anthesis 12. Oliverella
smooth to dentate or cleft. Fruits yellow, black, or – Corolla lobes erect, reflexed or rolled outwards at
red. Endosperm copious, embryo large, bicotylar, anthesis 10
the tips connate into a cone-like structure 10. Petals 4 11
(embryo solid in T. aphyllus). n ¼ 12. – Petals 5 12
An Andean genus of 12 spp.; Colombia to 11. Distinct corolla lobes ca. 1/4 length of the tube, cov-
southern Chile and adjacent Argentina. ered with irregularly branched hairs 4. Berhautia
98 Loranthaceae
22. Corolla slightly curved in bud, slightly inflated in the

– Distinct corolla lobes generally half as long as the tube middle, shortly hairy; stamens separate; style gla-
or longer, glabrous or occasionally covered with
brous 22. Taxillus
mostly simple hairs 6. Englerina
– Corolla straight-sided, tomentose; filaments short,
12. Corolla usually banded with 1–several contrasting
incurved, the anthers forming a central pollen mass;
colors, with vents opening below the corolla tip in
style hairy on lower half 23. Vanwykia
mature buds, the lobes often remaining erect 13
23. Stamens erect, slightly inclined at anthesis; flowers
– Corolla reddish, sometimes white or greenish towards
1–several in the axils, the pedicels arising separately;
extremities or spotted, with tips of buds swollen and
leaves alternate 18. Septulina
darkening at maturity, without vents below, opening
explosively with lobes generally reflexed, rolled out- – Stamens inrolled; flowers generally in sessile
wards or less often remaining erect 15 to shortly pedunculate umbels rarely 2–several
from the axils; leaves mostly opposite or subopposite
13. Distinct part of the petals shorter than the tube
16. Phragmanthera
2. Agelanthus
– Distinct part of the petals longer than the tube 14
14. Corolla buds straight, with a distinct tube developing
a V-split (other petals sometimes separating to this GENERA OF LORANTHACEAE OF AFRICA
point in dried specimens) 14. Oncocalyx AND MADAGASCAR
– Corolla buds bent at base (not always in S. curta from
NE Tanzania), with a very short tube split to base Polhill and Wiens, Mistletoes of Africa. Royal
without a distinct V 20. Spragueanella Botanic Gardens, Kew (1998), rev.
15. Petals reflexed or rarely erect 21. Tapinanthus
– Petals coiled outwards at anthesis 16
16. Anthers elongate, with equal thecae; style 1. Actinanthella Balle Fig. 25
slender, stigma small; corolla buds scarcely swollen
at apex 10. Moquiniella Actinanthella Balle, Bull. Séances, Acad. Roy. Sci. Colon.
– Anthers small, mostly fitting under top-shaped to 25: 1625 (1954).
peltate stigma, emarginate, with other thecae reduced; Loranthus Jacq. sect. Incrassati Sprague (1910).
corolla buds markedly swollen at apex
8. Globimetula
Small, branched shrubs without epicortical roots,
17. Flowers in extended spike or raceme 18
with short, stiff, spreading, simple or forked
– Flowers in clusters, umbellate, or capitate, occasion-
ally with a few flowers below the main head, candela- hairs. Leaves alternate. Flowers 1–3, axillary,
bra-like 20 very short-pedicellate; calyculus long, tubular,
18. Flowers covered in long, subsimple hairs circumscissile in fruit; petals 5, the distinct lobes
7. Erianthemum twice as long as the tube, mostly yellow-green,
– Flowers glabrous to tomentellous 19 developing wide vents; upper part of filament
19. Corolla yellow to red, without dark markings; tip of coiling at anthesis; anthers 4-loculate. Berry
corolla bud narrow, enclosing elongate anthers narrowly obovoid. n ¼ 9.
18. Oedina Two spp., SE and South Africa.
– Corolla pink or yellow-orange with dark glandular
spots at base of the lobes; tip of corolla bud obovoid,
enclosing small anthers with unequal thecae 2. Agelanthus Tiegh. Fig. 26
13. Oncella
20. Corolla opening radially, the lobes as long or dis- Agelanthus Tiegh., Bull. Soc. Bot. France 42: 246 (1895).
tinctly exceeding the tube; filaments inserted well up
the corolla lobes, elongate, often articulated and Loranthus Jacq. sect. Infundibuliformes (Engler) Sprague
breaking off near the middle 7. Erianthemum (1910).
– Corolla with short V-split at anthesis, the lobes Agelanthus Tiegh. sect. Acranthemum (Tiegh.) Polh. &
shorter than the tube; filaments attached ca. at the Wiens (1998).
base of the lobes, short, isodiametric, erect or inrolled Agelanthus Tiegh. sect. Agelanthus.
21 Agelanthus Tiegh. sect. Erectilobi (Sprague) Polh. &
21. Anthers not chambered; extensive epicortical roots Wiens (1998).
present, with secondary haustoria 22 Agelanthus Tiegh. sect. Longiflori (Engler) Polh. & Wiens
– Anthers locellate, the thecae subdivided into a series (1998).
of small chambers; stem from a single haustorial Agelanthus Tiegh. sect. Obtectiflori (Engler) Polh. &
attachment 23 Wiens (1998).
GENERA OF LORANTHACEAE OF AFRICA AND MADAGASCAR 99
Fig. 26. Loranthaceae. Agelanthus subulatus. A Flower-

ing node with leaves. B Flower bud. C Flower. D Stamen.
E Style-tip. F Fruits. G Seed. (Polhill and Wiens 1998,
drawn by C. Grey-Wilson)
Fig. 25. Loranthaceae. Actinanthella menyharthii. A
Flowering branchlet. B Hairs. C Mature bud. D Flower. E
Stamen. F Style-tip. G Fruit. (Polhill and Wiens 1998, linear. Berry ellipsoid to obovoid, smooth to
drawn by C. Grey-Wilson) warty, usually red when ripe. n ¼ 9.
Fifty-nine spp. in the Arabian Peninsula,
tropical Africa and South Africa.
Agelanthus Tiegh. sect. Purpuriflori (Engler) Polh. &
Wiens (1998). 3. Bakerella Tiegh.
Plants to 2 m, mostly with only a primary hausto- Bakerella Tiegh., Bull. Soc. Bot. France 42: 244 (1895).
rium; some with simple or irregularly branched Taxillus Tiegh. sect. Bakerella (Tiegh.) Balle (1955).
hairs. Leaves alternate to opposite, sometimes
clustered on short-shoots. Inflorescence a sessile Glabrous plants, some with epicortical roots and
to pedunculate head or umbel, in leaf axils or secondary haustoria in addition to the primary
sometimes terminal on short-shoots; petals 5, haustorium; branches mostly subterete, rarely
distinct, lobes mostly short, generally erect and quadrangular to 4-alate. Leaves decussate or
banded in different colors; mature buds with nearly so, petiolate or sessile, blade obovate,
subterminal vents, opening with a V-slit; base (sub)orbicular, elliptical to lorate, venation pin-
of bud sometimes dilated; anthers with 4 locules, nate to basal, often only the midrib obvious.
100 Loranthaceae
Inflorescences axillary, 1–5-flowered, generally face often scurfy. Leaves (sub)opposite, sessile to
short-pedunculate. Flowers sessile or pedicellate, generally petiolate. Inflorescence an erect, pedun-
each with a separate bract, (4)5-merous, red or culate umbel with 2–20 flowers; buds vented and
yellow (rarely white); stamens attached near petal basally dilated, with V-slit sometimes to the base;
tips; style slender, stigma large, distinct, globular petals 4, joined 1/5–2/3, red, yellow, orange or
to obovoid; calyculus persistent, rarely caducous, pink and white, distinct lobes erect, revolute or
fissuring in fruit. Fruit ellipsoid to obovoid, usu- reflexed; anthers 4-loculate. Berry urceolate to
ally blackish. Embryo bicotylar. n ¼ 9. obovoid, calyculus prominent, generally red.
Sixteen spp., endemic to Madagascar and n ¼ 9.
nearby islands, closely related to Taxillus. Twenty-five spp., various parts of tropical
Africa.
4. Berhautia Balle
7. Erianthemum Tiegh.
Berhautia Balle, Bull. Soc. Roy. Belg. 88: 133–146 (1956).
Erianthemum Tiegh., Bull. Soc. Bot. France 42: 241–272
Small plants with irregularly branched hairs; epi- (1895).
cortical roots lacking. Leaves alternate to subop- Loranthus Jacq. subgen. Erianthemum (Tiegh.) Balle
posite. Flowers in small axillary clusters; buds (1948).
straight, not basally dilated; petals 4, floral tube
pink, hairy, with short lateral V-slit, the distinct Plants 1–2 m, hairs stellate or dendritic, epicortial
lobes separate, erect, 1/3 as long as the floral tube; roots lacking. Leaves opposite or nearly so, or
filaments reflexed at anthesis. Berry pyriform, partly alternate or clustered on short shoots.
with prominent calyculus, red. n ¼ 9. Inflorescence a few-flowered head, or racemose
One spp., Berhautia senegalensis Balle, lim- or spicate, axillary, or on older nodes, or on leafy
ited to Senegal and Gambia. short shoots. Petals 5, joined less than halfway,
yellow to green with orange; bud basally dilated;
upper part of stamen breaking off when flower
5. Emelianthe Danser
opened, the filament coiling; anther 4-loculate.
Berry ovoid, with large calyculus, orange, reddish
Emelianthe Danser, Verh. Kon. Akad. Wetensch. Amster-
dam, Afd. Natuurk. II, 29(6): 1–128 (1933). or blue-green. n ¼ 9.
Loranthus Jacq. sect. Tetrameri Sprague (1910). Sixteen spp., eastern and southern Africa
Amyema sect. Tetrameri (Sprague) Balle (1955). from Ethiopia to the Cape Province of South
Africa; west to the Central African Republic.
Shrubs to 2 m, glabrous, without epicortical roots.
Leaves mostly alternate, also clustered on short- 8. Globimetula Tiegh.
shoots. Flowers 2–4, on short pedicels on the stem
or on short-shoots; petals 4, the brilliantly red, Globimetula Tiegh., Bull. Soc. Bot. France 42: 241–272
linear distinct lobes recurving; anthers 4-loculate. (1895).
Berry obovoid, purple. n ¼ 9.
One sp., Emelianthe panganensis (Engler) Plants 0.5–4 m, mostly with a single attachment,
Danser, northern Somalia to southern Tanzania occasionally scandent with many secondary
and southern Ethiopia, west to Uganda. haustoria, mostly hairless. Leaves opposite, sub-
opposite, or ternate. Inflorescence a 2–20-flow-
6. Englerina Tiegh. ered umbel. Petals 5, pink or red, sometimes
with white or green; bud apex swollen, often
Englerina Tiegh., Bull. Soc. Bot. France 42: 241–272 darkening, basally dilated; bud splitting unilater-
(1895). ally more than halfway down; stamens coiling
at anthesis, 4-loculate. Berry red to yellow,
Plants 0.5–2 m, glabrous or short-hairy, lacking depressed-globose to ellipsoid. n ¼ 9.
epicortical roots; hairs simple or nearly so, sur- Thirteen spp., tropical Africa.
9. Helixanthera Lour. Fig. 27
Helixanthera Lour., Fl. Coch. 1: 142 (1790).
Small plants lacking epicortical roots, glabrous

in Africa, elsewhere sometimes scurfy and with
small hairs. Internodes terete, flattened or angu-
lar; leaves opposite to alternate. Inflorescence a
terminal and/or axillary raceme or spike. Petals
4–7, distinct, white, yellow or red, not banded;
stamens erect; anther 2- or 4-loculate, immobile,
sometimes partitioned transversely; style simple
or constricted at mid-level; stigma capitate.
Berries spherical to ellipsoid, smooth or verru-
cose. n ¼ 9.
Forty-five spp., tropical Africa and Asia, to
Sulawesi.
10. Moquiniella Balle
Moquiniella Balle, Bull. Séances Acad. Roy. Sci. Colon. 25: Fig. 27. Loranthaceae. Helixanthera kirkii. A Flowering
1628 (1954). and fruiting branchlet. B Flower bud. C Flower. D and E
Petal with stamen, front and side views. F Section of
Plants small, with short, thick, branched hairs; gynoecium. G Fruit. (Polhill and Wiens 1998, drawn by
epicortical roots absent. Leaves alternate to sub- C. Grey-Wilson)
opposite or ternate. Inflorescence an umbel, axil-
lary or terminal on short shoots, few-flowered.
Petals 5, red, orange, or yellow, with short lateral 12. Oliverella Tiegh.
V-slit; buds straight, with somewhat dilated base;
lobes strongly coiled at anthesis; anthers long and Oliverella Tiegh., Bull. Soc. Bot. France 42: 241–272
narrow, 4-loculate. Berry red, ellipsoid, calyculus (1895).
small. n ¼ 9.
One sp., Moquiniella rubra (A. Sprengel) Small plants with simple, spreading hairs; epicor-
Balle; extreme coastal South Africa and adjacent tical roots lacking. Leaves opposite to alternate.
Namibia. Inflorescence a pedunculate umbel, one per axil,
often many-flowered. Bud slightly curved, apex
somewhat swollen, with basal vents, tubular
11. Oedina Tiegh.
part green; petals 5, the upper parts connivent,
red at least in part, inrolled at anthesis; filament
Oedina Tiegh., Bull. Soc. Bot. France 42: 241–272 (1895).
becoming coiled; anthers 4-loculate. Berry
obovoid, red, with prominent, short calyculus.
Plants to 2 m or more; epicortical roots lacking,
n ¼ 9.
with stellate to dendritic hair cover. Leaves
Three spp. in E and South-Central Africa.
mostly opposite or nearly so, rarely clustered.
Inflorescence a raceme or spike, axillary and/or
on older nodes. Flowers 5-merous, yellow to red, 13. Oncella Tiegh.
the tube reaching the middle; buds with vents
below the middle; petal lobes erect; anthers Oncella Tiegh., Bull. Soc. Bot. France 42: 241–272 (1895).
4-loculate, filaments coiling and often breaking
off at anthesis. Berry (at least in most species) Small plants with stellate and dendritic hairs;
blue-green, ca. ovoid. n ¼ 9. epicortical roots lacking. Leaves opposite or
Four spp., East Central Africa. nearly so. Inflorescence a raceme. Petals 5, orange
102 Loranthaceae
to red or pink, the tube half as long as the

(vented) bud, weakly explosive, with basal dila-
tion; apex rounded or blunt; upper part of fila-
ment coiling and breaking off; anthers 4-loculate.
Berry ellipsoid, white to red, sometimes turning
black. n ¼ 9.
Four spp. in eastern Africa.
14. Oncocalyx Tiegh. Fig. 28
Oncocalyx Tiegh., Bull. Soc. Bot. France 42: 241–272

(1895).
Oncocalyx Tiegh. sect. Longicalyculati (Engler) Wiens &
Polh. (1998).
Small plants, glabrous or with short, spreading,

simple hairs; epicortical roots lacking. Leaves
mostly alternate. Flowers axillary or in 2–6-flow- Fig. 28. Loranthaceae. Oncocalyx fischeri. A The mistle-
ered, short umbels; calyculus often tubular; bud toe on its host branches. B Bract, calyculus and ovary
longitudinally sectioned. C Anther. D Style and stigma.
sometimes basally swollen; vented when mature; (Engler 1915)
petals 5, partly joined below, opening with a lat-
eral V-slit, at least partly yellow, or banded red
with white or green; anthers 4-loculate, coiled at
anthesis. Fruit red, mostly obovoid, calyculus
often prominent. n ¼ 9.
Thirteen spp., southern Africa and East
Africa to Arabia.
15. Pedistylis Wiens
Pedistylis Wiens, Bothalia 12: 421 (1978).
Plants probably >2 m, glabrous, the single haus-

torial connection reaching to 1 m in diameter.
Leaves paired or mostly so. Flowers 2 or 3 per
inflorescence, clustered or umbellate on a short
peduncle; petals 5, joined halfway, the distinct
lobes reflexing; anthers 4-loculate. Berries ellip-
soid, red. n ¼ 9.
One sp., Pedistylis galpinii (Schinz ex Spra-
gue) Wiens; NE Transvaal, Swaziland, SE Zim-
babwe and southern Mozambique.
16. Phragmanthera Tiegh. Fig. 29 Fig. 29. Loranthaceae. Phragmanthera usuiensis subsp.
usuiensis. A Flowering node and leaf. B Trichomes from
Phragmanthera Tiegh., Bull. Soc. Bot. France 42: 241–272 surface of twig. C Tip of young flower bud. D Same at
(1895). maturity, with vents open. E Flower. F Detail of corolla
lobe. G Surface of corolla showing trichomes. H Stamen.
Phragmanthera Tiegh. sect. Eubracteatae (Engler) Polh. &
I Style-tip. J Fruit. (Polhill and Wiens 1998, drawn by
Wiens (1998). C. Grey-Wilson)
Phragmanthera Tiegh. sect. Lepidotae (Engler) Polh. &

Wiens (1998).
Phragmanthera Tiegh. sect. Rufescentes (Engler) Polh. &
Wiens (1998).
Plants often large and pendent, lacking epicortical

roots, with scaly and branched hairs at least when
young. Leaves opposite or nearly so, rarely ter-
nate. Inflorescence a short-stalked or sessile
umbel, or flowers 2–several in leaf axils. Petals 5
(6), mostly red or orange, the connate parts lon-
ger than the distinct, erect or reflexed lobes; bud
apex fusiform to globular; base often dilated, tube
vented and later split laterally, the V-shaped slit
at least halfway down to the base; anthers narrow,
with 4 transversely partitioned locules, filament
inrolled at anthesis. Berry ellipsoid to obovoid,
blue or blue-green. n ¼ 9.
Thirty-four spp., Arabia and tropical Africa.
17. Plicosepalus Tiegh. Fig. 30

Fig. 30. Loranthaceae. Plicosepalus curviflorus. A Young
Plicosepalus Tiegh., Bull. Soc. Bot. France 41: 504 (1894). plant with epicortical roots. B Flowering branch. C Base of
petals showing stamen insertion. D Anther. E Gynoecium.
(Polhill and Wiens 1998, drawn by C. Grey-Wilson)
Plants of various sizes (a few cm to several m),
mostly glabrous; epicortical roots present. Leaves
paired, alternate, or irregular, often clustered on anthers 4-loculate. Berry red, ellipsoid, hairy.
short-shoots, venation palmate. Inflorescence a n ¼ 9.
few-flowered umbel, axillary or terminating Two spp., Western Cape Province of South
short-shoots; bud slightly or markedly curved, Africa and adjacent Namibia.
mostly red or yellow, calyculus occasionally split
at anthesis; petals 5, each with 2 rows of oblique
19. Socratina Balle
internal folds where connivent; upper parts of
petals reflexing and often twisting at anthesis;
Socratina Balle, Adansonia II, 4: 130 (1964).
anthers 4-loculate. Berries ellipsoid or urceolate,
red or yellow. n ¼ 9.
Plants with multicellular, whitish to brownish,
Twelve spp., Middle East and Arabia, espe-
variously persistent hair cover; haustorial connec-
cially E Africa, some in South Africa.
tion unknown; internodes more or less terete, S.
bemarivensis with leafy short shoots. Leaves alter-
18. Septulina Tiegh. nate to decussate, narrowly oblong to broadly
elliptical or orbicular, venation somewhat
Septulina Tiegh., Bull. Soc. Bot. France 42: 263 (1895). obscure, mostly basal. Inflorescences axillary or
Taxillus Tiegh. sect. Septulina (Tiegh.) Balle (1955). perhaps terminal on the short shoots. Flowers
solitary and sessile or pedicellate, or in very
Plants to 1 m in diameter, covered by stellate and short dichasia, each subtended by a small bract;
dendritic hairs, epicortical roots lacking. Leaves calyculus entire or shallowly dentate; bud hairy,
alternate or clustered. Flowers short-pedicellate, swollen subterminally, apex obtuse or nearly so;
arising 1-several in leaf axils; buds with subapical, petals 5, hairy on upper, internal faces, anthers
short vents; petals 4, hairy, red and green, the not septate, 4-loculed; style slender, short-hairy in
tube splitting laterally to the base when mature; mid-section. Embryo dicotylous. n ¼ 9.
104 Loranthaceae
Two spp., endemic to SW Madagascar. About thirty-five spp., Sri Lanka to China,
Philippines, Borneo, and Japan, one sp. in coastal
Kenya.
20. Spragueanella Balle
Three groups of African species were united
in Taxillus at one time (Balle 1955), as sect.
Spragueanella Balle, Bull. Séances Acad. Roy. Sci. Colon.
25: 1619–1635 (1954). Bakerella (Tiegh.) Balle, sect. Remoti (Sprague)
Balle, and sect. Septulina (Tiegh.) Balle, but these
Small glabrous plants lacking epicortical roots. are now recognized as separate genera (Bakerella
Leaves subopposite. Inflorescence a short-pedun- Tiegh., Vanwykia Wiens, and Septulina Tiegh.,
culate umbel. Buds basally dilated and curved, tip respectively). See also entry to this genus under
narrowly clavate, vented, yellow to red; petals 5; Loranthaceae of Eurasia.
stamens with inrolled filaments at anthesis,
anthers linear, 4-loculate. Berry obovoid. n ¼ 9. 23. Vanwykia Wiens
Two spp. in E Africa.
Vanwykia Wiens, Bothalia 12: 421–423 (1978).
21. Tapinanthus (Blume) Reichb., nom. gen. con-
serv. # 2074a. Plants to 1.5 m, with stout epicortical roots
bearing secondary haustoria, covered by stellate
Tapinanthus (Blume) Reichb., Repert. Herb.: 73 (1841). and dendritic hairs. Leaves alternate to opposite.
Inflorescence a short-stalked umbel of 2–6 sessile
Plants to 2 m, epicortical roots lacking, twigs flowers, axillary and on older nodes. Petals (4)5,
glabrous to short-hairy with small simple hairs. green becoming reddish, tomentose, developing a
Leaves mostly opposite. Inflorescence a short- short V-slit, distinct lobes short; bud straight;
pedunculate umbel, axillary or nodal on older anthers clustered to form a central mass, each
growth. Petals 5, the distinct lobes much shorter 4-loculate. Berry red, cylindrical, hairy. n ¼ 9.
that the tube, usually pink to purplish, the Two spp., East and SE Africa.
expanded bud apex greenish to white, becoming
dark, base dilated; anthers 4-loculate, short. Berry KEY TO THE GENERA OF LORANTHACEAE
oblong-ellipsoid to globose, calyculus prominent, OF AUSTRALIA AND NEW ZEALAND
usually red when ripe. n ¼ 9.
Thirty spp. in tropical and southern Africa, Barlow, Flora Males. I, 13: 209–401 (1997).
one sp. extending to N Yemen. 1. Terrestrial trees or shrubs (Australia) 2
– Parasites on branches of woody plants (Australia or
22. Taxillus Tiegh. New Zealand) 3
2. Inflorescence triadic; fruit a dry, winged nut; Western
Australia 12. Nuytsia
Taxillus Tiegh., Bull. Soc. Bot. France 42: 256 (1895).
– Inflorescence monadic; fruit drupaceous; New South
Wales 4. Atkinsonia
Small shrubs with epicortical roots, covered with 3. Flowers 5- or 6-merous (rarely 4-merous in
stellate, dendritic, or simpe hairs. Leaves alter- Amyema); Australia and elsewhere but not New Zeal-
nate to opposite. Inflorescence an umbel or clus- and (except possibly Muellerina celastroides on Bay
ter, (occasionally solitary or sessile), these of Islands) 8
axillary or terminal on short shoots. Petals 4 or – Flowers 4-merous (rarely 5-merous in Tupeia); New
5, the bud often curved, the tip clavate, with Zealand 4
lateral V-slit, often opening explosively; petals 4. Each flower with three persistent bracts; anther with
acute, apiculate connective 0.3 mm long; extinct
yellow or red and green, the distinct lobes erect 14. Trilepida
or recurved; stamens erect, the anthers 4-loculate. – Floral bracts, if present, caducous; anthers
Berry ovoid to obovoid, usually reddish, calycu- lacking long apiculate connective; North and South
lus prominent. n ¼ 9. Islands 5
GENERA OF LORANTHACEAE OF AUSTRALIA AND NEW ZEALAND 105
5. Dioecious; epicortical roots lacking; staminate flower Plants glabrous or minutely scurfy, with epicor-
without calyculus 15. Tupeia tical roots and secondary haustoria. Leaves
– Flowers bisexual; epicortical roots present; decussate, oblong to nearly ovate, rounded api-
flowers with calyculus 6 cally but often with acute, deciduous apiculus
6. Flowers sessile 13. Peraxilla when young, base acuminate, petiole 3–10 mm
– Flowers pedicellate 7 long, venation curvinervous. Inflorescences axil-
7. Inflorescences determinate (i.e., with terminal lary, with 2–5 basal pairs of scale leaves, each
flower), monadic throughout; style straight
1. Alepis inflorescence a spike of 2–11 pairs of decussate
– Inflorescence indeterminate, triadic at least basally; flowers and a single terminal flower; lateral flow-
style twisted 9. Ileostylus ers pedicellate, each subtended by a deciduous
8. Inflorescence capitate, with 2/3 sessile triads; two bract and 2 deciduous bracteoles. Flowers
central bracts foliaceous, covering the young flowers 4-merous, bisexual, basally gamopetalous; petals
8. Diplatia ca. 13–20 mm long, usually yellow; anthers
– Inflorescence otherwise, without foliaceous bracts 9 oblong, basifixed, immobile; style articulate near
9. Stamens dorsifixed, versatile; inflorescence terminal the base, stigma thick, capitate. Fruit urceolate,
11. Muellerina with basal style remnant. Seedling cryptocotylar.
– Stamens basifixed, immobile; inflorescences mostly n ¼ 12.
axillary 10
One sp., A. flavida (Hook. f.) Tiegh., endemic
10. Petals 6 11
to New Zealand.
– Petals 4 or 5 14
11. Inflorescence a pedunculate, many-rayed umbel of
triads (reduced in some to capitula or single flowers); 2. Amyema Tiegh.
n¼9 2. Amyema
– Inflorescence racemose with pairs of Amyema Tiegh., Bull. Soc. Bot. France 41: 499 (1894).
pedunculate triads (in some, variously reduced);
n ¼ 12 12
12. Leaves mostly linear to terete; inflorescence a 2-flow- Plants with opposite, verticillate, or scattered
ered umbel (sometimes reduced to a single flower); leaves; epicortical roots present or absent. Inflo-
anthers linear 10. Lysiana rescence axillary or rarely emerging from the
– Leaves otherwise; inflorescence (at least basally a internodes or even from epicortical roots, each a
raceme of pedicellate triads (sometimes reduced) pedunculate, many-rayed umbel of triads/tetrads
13 or reduced versions as capitula or individual
13. Mature buds dilated in the middle; fruit ellipsoidal to flowers; each flower mostly with a single bract.
globular 3. Amylotheca
Petals 4, 5, or 6, usually separate at anthesis but
– Mature buds slender, not dilated; fruit urceolate to
nearly globular 6. Decaisnina sometimes coherent in the lower part; anthers
14. Inflorescence and ovary brown-tomentose; inflores- basifixed, immobile, 2- or 4-loculate; style usually
cence 2-flowered, flowers sessile 5. Benthamina articulate basally, stigma distinct, capitate. Fruit
– Inflorescence and ovary glabrous; inflorescence a ellipsoid-(ob)ovoid. n ¼ 9.
raceme, spike, or an umbel of triads or tetrads 15 About 90 spp., SE Asian mainland to Austra-
15. Inflorescence mostly a raceme or spike lia and the western Pacific as far as Samoa.
7. Dendrophthoe
– Inflorescence mostly umbellate, with various num-
bers of rays of triads or tetrads 2. Amyema 3. Amylotheca Tiegh.
Amylotheca Tiegh., Bull. Soc. Bot. France 41: 261–265

(1894).
GENERA OF LORANTHACEAE OF AUSTRA-
LIA AND NEW ZEALAND Glabrous shrubs with epicortical roots; leaves
opposite. Inflorescence a subumbellate raceme
Barlow, Austral. J. Bot. 14: 421–499 (1966), rev. of triads, the central flower of triads sessile, lat-
eral flowers pedicellate; sometimes a simple
1. Alepis Tiegh. raceme or 2-flowered umbel. Mature bud dilated
in the middle; petals 6, at anthesis united to the
Alepis Tiegh., Bull. Soc. Bot. France 41: 604 (1894). middle or higher; anthers linear, basifixed; style
106 Loranthaceae
tent, small basal scales, each a raceme of 2 or 3

pairs of pedunculate flowers, these subtended by
one bract and two bracteoles. Flowers bisexual,
choripetalous; bud ovoid with more or less acute
apex; petals 6, 6–8 mm long, yellow; anthers
oblong, on short filaments, acute, dorsifixed, ver-
satile, in 2 series. Fruit ovoid, ca. 12 mm long, the
endosperm deeply grooved; seedling probably
cryptocotylar. n ¼ 12.
One sp., A. ligustrina (A. Cunn. ex Lindl.) F.
Muell., endemic to the Blue Mountains, New
South Wales. This is one of three basal Lorantha-
ceae, the others being Gaiadendron and Nuytsia.
While the other two have inflorescences with
triads, its inflorescences are made up of bracteo-
late monads.
5. Benthamina Tiegh.
Benthamina Tiegh., Bull. Soc. Bot. France 42: 85 (1895).
Glabrous plants except for the densely, short

brown-tomentose inflorescence and ovary; epi-
cortical roots and secondary haustoria present.
Leaves decussate, elliptical to ovate, recurved api-
cally, abruptly contracted at the base. Inflores-
cences axillary, several at the nodes,
pedunculate, 2-flowered. Flowers bisexual, sessile
and with one bract each; anthers linear, basifixed,
Fig. 31. Loranthaceae. Atkinsonia ligustrina. A Flowering immobile. n ¼ 9.
branch. B Bud. C Flower with bracteate pedicel. D One sp., B. alyxifolia (F. Muell. ex Benth.)
Perianth segment with stamen. E Anther. F Style. G
Fruit. H Fruit, longitudinal section. I Fruit, cross section. Tiegh., SE Queensland and NE New South Wales.
J Embryo. K Seedling plant, showing the fibrous roots.
L Floral bracts with bracteoles, after the fruits have fallen.
(Blakely 1922, drawn by author) 6. Decaisnina Tiegh.
Decaisnina Tiegh., Bull. Soc. Bot. France 42: 435 (1895).

articulate above the base, its base pyramidal.
Berry ellipsoidal or globular. n ¼ 12. Plants with epicortical roots and secondary
Five spp., eastern Australia, New Guinea, and haustoria. Leaves opposite, venation pinnate.
Melanesia. Inflorescence a raceme of several pairs of triads,
axillary, flowers sessile or lateral ones of triads
4. Atkinsonia F. Muell. Fig. 31 short-pedicellate. Mature bud slender; petals 6, at
anthesis distinct or connivent at the base; anthers
Atkinsonia F. Muell., Fragm. 5: 34 (1865). narrow, basifixed, acute; style articulate at or
above the base. Fruit urceolate to nearly globular.
Low, glabrous, evergreen, terrestrial shrubs; n ¼ 12.
internodes and inflorescence axis angular. Leaves 25–30 spp., Philippines to northern Australia
decussate, lanceolate, petiole 2 mm long. Inflores- and Tahiti; D. forsteriana eastwards to the Mar-
cence solitary, axillary, with a few pairs of persis- quesas (Barlow and Schodde 1993).
GENERA OF LORANTHACEAE OF AUSTRALIA AND NEW ZEALAND 107
7. Dendrophthoe Mart. Plants lacking epicortical roots. Leaves linear, flat

with pinnate venation or terete, decussate (some-
Dendrophthoe Mart., Flora 13: 109 (1830). times clustered). Inflorescence axillary, a pedun-
culate or sessile 2-flowered umbel or a single
See entry under Eurasian genera. flower, each flower with a single bract clasping
the ovary. Flowers bisexual, gamopetalous,
8. Diplatia Tiegh. curved in bud; anthers basifixed on distinct fila-
ments, linear, acute, 4-locular; style articulate just
Diplatia Tiegh., Bull. Soc. Bot. France 41: 501 (1894). above the base. Fruit ovoid, ellipsoid, or truncate,
variously colored. n ¼ 12.
Mostly glabrous plants (one sp. with tomentum on Six spp., endemic to Australia.
ovary and the inside of floral bracts), lacking epi-
cortical roots but with extensive endophytic
11. Muellerina Tiegh.
strands in host tissues. Leaves decussate, lanceo-
late to oblong, venation nearly parallel to curvi-
Muellerina Tiegh., Bull. Soc. Bot. France 42: 25 (1895).
nervous. Inflorescences capitate, made up of
(mostly) 2 sessile triads, the central bracts of triads
Plants glabrous or minutely brown-tomentose on
enlarged and foliaceous, oblong to ovate, enclosing
the inflorescence, with epicortical roots and
the flowers and basally connate in early develop-
secondary haustoria. Leaves decussate, linear,
ment; bracteoles small, narrow, deciduous. Flow-
oblong, or elliptical. Inflorescence terminal,
ers bisexual; petals 5, choripetalous; anthers
often on short lateral stems and then seemingly
basifixed, immobile; style articulate basally. Fruit
axillary, being a raceme of 1–6 pairs of peduncu-
ellipsoidal, with truncate apex. n ¼ 9.
late triads or single flowers, central flower of
Three spp., endemic to Australia.
triads sessile, other flowers pedicellate, all flowers
choripetalous, bisexual, 5-merous, curved in bud.
9. Ileostylus Tiegh. Stamens unequal, anthers bilocular, dorsifixed,
versatile. Fruit pyriform. n ¼ 11.
Ileostylus Tiegh., Bull. Soc. Bot. France 41: 483 (1894). Four spp., endemic to E Australia.
Moderately small plants, glabrous, innovations

12. Nuytsia R. Brown Fig. 32
with a few pairs of deciduous basal scales, inter-
nodes flattened and somewhat carinate when
Nuytsia R. Brown, J. Geogr. Soc. 1: 17 (1831).
young, becoming terete but retaining 2 ridges;
epicortical roots and secondary haustoria pres-
Terrestrial trees or large shrubs, parasitic on
ent. Leaves decussate, oblong to (ob)ovate. Inflo-
roots of numerous spp., occasionally to 12 or
rescence emerging pseudo-endogenously from a
even 15 m high. Leaves narrowly lanceolate,
brown, corky cover, variable in composition,
usually glaucous, rounded to acute apically,
mostly indeterminate and consisting of peduncu-
attenuate and sessile basally, decussate to scat-
late triads topped by pedicellate monads, some-
tered (rarely verticillate), venation pinnate.
times with a single, terminal flower. Flowers
Plants monoecious. Inflorescences axillary and
bisexual, unisexual, or intermediate, 4-merous;
terminal, each a (sometimes branched) indeter-
anthers basifixed, immobile, oblong; style con-
minate raceme with to 25 pairs of pedunculate
torted, stigma small, capitate. Fruit ellipsoidal to
triads, central flower bisexual, lateral ones sta-
nearly globular. n ¼ 11.
minate and bearing stylodia; each flower sub-
One sp., I. micranthus (Hook. f.) Tiegh.,
tended by a bract/bracteole and sessile; petals
endemic to New Zealand, including Stewart
6, choripetalous, golden yellow; stamens in
Islands; a small population on Norfolk Island.
2 series, anthers dorsifixed on distinct filaments;
style slender, somewhat persistent. Fruit a dry,
10. Lysiana Tiegh. strongly 3-winged nut; embryo slender, germi-
nation epigaeus, seedling phanerocotylar.
Lysiana Tiegh., Bull. Soc. Bot. France 41: 599 (1894). n ¼ 12.
108 Loranthaceae
13. Peraxilla Tiegh.
Peraxilla Tiegh., Bull. Bot. Soc. France 41: 500 (1894).
Robust, glabrous plants with epicortical roots and

secondary haustoria; internodes terete to qua-
drangular. Leaves elliptical to ovate or rhomboi-
dal, venation essentially pinnate. Inflorescences
axillary, rarely terminal on short lateral branches,
each with 1–5 flowers and a single terminal
flower, emerging from corky crater; lateral flow-
ers subtended by a deciduous bract; bracteoles
lacking. Flowers bisexual, 4-merous, red, orange,
or (rarely) yellow; anthers linear, basifixed on
short filaments, immobile, apex acute; style artic-
ulate just above the base. n ¼ 12.
Two spp., endemic to New Zealand, fre-
quently but not exclusively on Nothofagus.
14. Trilepidea Tiegh.
Trilepidea Tiegh., Bull. Soc. Bot. France 42: 28 (1895).
Glabrous plants, young internodes flattened dis-

tally, becoming terete; innovations basally with
1–3 pairs of spaced, decussate, acute scales; epi-
cortical roots unknown. Leaves oblong, ovate, or
rhomboidal, basally attenuate, with alate petiole
to 5 mm long; venation pinnate. Flowers bisexual.
Inflorescences axillary, indeterminate, each a
few-flowered raceme with basal pairs of decussate
scale leaves. Flowers each with one persistent
bract and 2 bracteoles; petals 4, said to be gamo-
petalous but probably coherent; anthers narrowly
Fig. 32. Loranthaceae. Nuytsia floribunda. A Portion of
oblong, basifixed, immobile, bilocular, apex
flowering branch. B Common obtuse leaf. C Triad of buds. acute; style articulate basally. Fruit unknown.
D Flower. E Anther. F Calyx and style. G Portion of One sp., T. adamsii (Cheesem.) Tiegh.,
fruiting branch. H Fruit removed of some bracts. I Seed. extinct, New Zealand (North Island).
J Longitudinal section of seed. K Cross section of seed.
L Embryo showing three cotyledons. M Seedling. N Para-
sitism of Nuytsia (a host, b root of Nuytsia with connec- 15. Tupeia Cham. & Schlecht.
tion to haustorium, c). O Longitudinal section of a carrot
encircled by haustorium. (Blakely 1922, drawn by the
author) Tupeia Cham. & Schlecht., Linnaea 3: 203 (1828).
Moderately small plants lacking epicortical roots,

One sp., Nuytsia floribunda (Labill.) R. Br. ex glabrous or with some short, simple hairs; inter-
G. Don, endemic to SW Western Australia. nodes pale-colored, somewhat flattened when
This is a well-known tree in Australia, even young, becoming terete, innovations with basal
having a botanical journal named after it, and scale-leaves. Leaves lanceolate to ovate or rhom-
producing great masses of golden flowers. It is boidal, decussate, more or less attenuate and
regarded as sister to all other Loranthaeae, sharing acute apically, attenuate basally. Dioecious.
its basal status with Atkinsonia and Gaiadendron. Inflorescences terminating leafy innovations,
KEY TO THE GENERA OF LORANTHACEAE OF EURASIA 109
determinate, each a raceme with several pairs of 8. Petals distinct 1. Amyema

pedicellate monads often with some pedicellate – Petals connate to the middle or higher 9
triads below and a single terminal flower, all 9. Inflorescence in reality a subumbellate raceme of
flowers pedicellate and usually lacking bracts; triads tightly crowded at the apex of the axis, with
staminate flower 4(rarely 5)-merous, lacking narrow involucral segments developed from the
bracts of the outer flowers and connate with the ped-
calyculus, choripetalous; stamens inserted on icels and rays 13. Lampas
lowest part of petals, anthers bilocular, basifixed; – Inflorescence distinctly capitate, the flowers inserted
pollen spherical, minutely spinescent; pistillate on a flat receptacle, with broad involucral segments
flower 4-merous, choripetalous, style straight, developed from non-fertile bracts 10
with large, capitate stigma. Fruit globular, more 10. Inflorescence triads in the axils of enlarged bracts,
or less translucent, embryo bicotylar, seedling with each flower surrounded by 3 smaller bracts
phanerocotylar. n ¼ 11. 23. Thaumasianthes
One sp., T. antarctica (Forst. f.) Cham. & – Inflorescence triads not in the axils of enlarged bracts
(except the outer triads), with each flower subtended
Schlecht., endemic to New Zealand. by a single small bract 14. Lepeostegeres
11. Involucral bracts subtending the individual flowers
KEY TO THE GENERA OF LORANTHACEAE 10. Elytranthe
OF EURASIA – Involucral bracts tightly enclosing the whole inflores-
cence 15. Lepidaria
N.B. A single species of the African genus Tapi- 12. Flowers in simple dichasia (triads or rarely tetrads),
nanthus occurs in Yemen (see under African those in most species aggregated into larger racemose
genera). or umbellate inflorescences 13
– Flowers single in the inflorescences (racemes, spikes,
1. Inflorescence a capitulum of (3–)6 sessile flowers sur- umbels, capitula or solitary flowers 19
rounded by (3–)5 basally connivent, foliaceous bracts; 13. Petals connate to the middle or higher (sometimes
Sri Lanka to SE continental Asia 24. Tolypanthus with the corolla tube deeply split on one side) 14
– Inflorescence otherwise, or flowers solitary and ses- – Petals distinct completely or almost to the base
sile 2 (sometimes coherent for some time after anthesis)
2. Inflorescence lacking, the solitary flowers sessile at 17
the nodes 11. Helicanthes 14. Anthers dorsifixed 17. Loxanthera
– Inflorescences present 3 – Anthers basifixed 15
3. Inflorescences developing in a shallow depression 15. Inflorescence a subumbellate raceme of triads tightly
under a bubble-like calyptra of one piece formed crowded at the apex of the axis, with narrow involu-
from the stem periderm and falling and rupturing cral segments developed from the bracts of the outer
irregularly as the inflorescence develops underneath flowers and connate with the pedicels and rays
it 5. Cyne 13. Lampas
– Inflorescence externally visible from an early stage, – Inflorescence umbellate or racemose but lacking an
not developing under a calyptra 4 involucre of enlarged bracts 16
4. Inflorescence a head with an involucre of enlarged 16. Inflorescence umbellate 1. Amyema
imbricate or valvate bracts completely or partially – Inflorescence racemose 2. Amylotheca
enclosing the flowers 5
17. Inflorescence umbellate, sometimes contracted to a
– Inflorescence not a head, or if so, with floral bracts head 1. Amyema
not enlarged and imbricate or valvate, nor forming an
involucre around the entire inflorescence 12 – Inflorescence racemose 18
5. Involucral bracts 2, connate at the margins 6 18. Inflorescence a raceme with whorls of triads
6. Dactyliophora
– Involucral bracts 4 or more, distinct, usually imbicate
7 – Inflorescence a raceme with decussate triads
7. Decaisnina
6. Flowers in the inflorescence 6 in 2 opposite triads,
sessile 9. Distrianthes 19. Petals connate to the middle or higher (sometimes
with the corolla tube deeply slit on one side) 20
– Flowers in the inflorescence 8–12 in 2 opposite rows,
pedicellate and with a bract at the apex of each pedicel – Petals distinct completely or almost to the base
19. Papuanthes (sometimes coherent for some time after anthesis)
27
7. Flowers in the inflorescence (at least the outer ones)
grouped in triads 8 20. Corolla 6-merous 21
– Flowers in the inflorescence not grouped in triads 11 – Corolla 4- or 5-merous 25
110 Loranthaceae
21. Bracts 3 under each flower, sometimes partly united sometimes coherent in the lower part; anthers
22 basifixed, immobile, 2- or 4-loculate; style usually
– Bracts single under each flower 24 articulate basally; stigma distinct, capitate. Fruit
22. Inflorescence a solitary flower on a short (sometimes ellipsoid-(ob)ovoid. n ¼ 9.
articulate) pedicel 21. Sogerianthe About 90 spp., SE Asian mainland to Austra-
– Inflorescence a spike or a raceme 23 lia and the western Pacific as far as Samoa.
23. Inflorescence axis decussately flattened, with the flow-
ers borne in hollows 10. Elytranthe
– Inflorescence axis terete or quadrangular, with the 2. Amylotheca Tiegh.
flowers not borne in hollows 18. Macrosolen
24. Flowers strongly reflexed upwards from a vertical Amylotheca Tiegh., Bull. Soc. Bot. France 41: 261–265
axis; corolla thick, more than 60 mm long (1895).
25. Trithecanthera
– Flowers not reflexed on the axis; corolla thin, less than Robust plants with epicortical roots and second-
60 mm long 2. Amylotheca ary haustoria. Leaves mostly decussate, venation
25. Fruit obovoid, club-like, distincty stipitate pinnate. Inflorescences axillary, basically a
20. Scurrula raceme of decussate pairs of pedunculate triads
– Fruit ovoid or ellipsoid, not stipitate 26 (sometimes variously reduced), each flower with
26. Inflorescence racemose (sometimes few-flowered and a single bract. Flowers 6-merous, gamopetalous;
subumbellate); corolla 5- or rarely 4-merous, regular
or slightly zygomorphic; leaves mostly alternate anthers basifixed, immobile; style articulate
8. Dendrophthoe above the base; stigma usually capitate. Fruit
– Inflorescence a few-flowered umbel; corolla ellipsoid to globular, usually with persistent stylar
(in Malesia) 4-merous, zygomorphic; leaves opposite base. n ¼ 12.
22. Taxillus Four spp., Thailand and Peninsular Malaysia
27. Anthers dorsifixed, versatile 4. Cecarria E and S to New Guinea, Australia, New Caledonia,
– Anthers basifixed, immobile 28 and New Hebrides.
28. Inflorescence a simple umbel or solitary flower
1. Amyema
– Inflorescence a raceme, spike, or contracted to a head 3. Barathranthus Miquel
29
29. Inflorescence sessile, capitate, a very condensed spike Barathanthus Miquel, Fl. Ind. Bat. 1, 1: 834 (1856).
without involucre 3. Barathranthus
– Inflorescence a raceme or spike 30 Sparsely branched plants with epicortical roots
30. Flowers hermaphrodite; anthers linear and secondary haustoria; internodes terete or
12. Helixanthera quadrangular. Leaves decussate to displaced,
– Flowers mostly unisexual; anthers globose or subglo- sometimes alternating with small, reduced ones.
bose 16. Loranthus
Inflorescence a capitulum or much abbreviated
spike, the flowers placed in small cavities, each
GENERA OF LORANTHACEAE OF EURASIA
flower with a single bract. Flowers bisexual (at
least B. productus), or unisexual when plants
1. Amyema Tiegh. dioecious (B. axanthus), small; petals 4, choripe-
talous; anthers basifixed, immobile; style straight,
Amyema Tiegh., Bull. Soc. Bot. France 41: 499 (1894); stigma small. Fruit ellipsoid to globose.
Barlow, Blumea 36: 293–381 (1992), rev.
Four spp., Sri Lanka, SE to Indochina and
Malesia, 2 spp. reaching Borneo and Java.
Plants with opposite, verticillate, or scattered
leaves; epicortical roots present or absent. Inflor-
escences axillary, rarely emerging from the inter- 4. Cecarria Barlow
nodes or even from epicortical roots, each a
pedunculate, many-rayed umbel of triads/tetrads Cecarria Barlow, Brittonia 25: 28, 34 (1973).
or reduced versions as capitula or individual
flowers; each flower mostly with a single bract. Plants with opposite leaves with curvilinear veins.
Petals 4, 5, or 6, usually separate at anthesis but Inflorescence an axillary 2-flowered umbel, each
GENERA OF LORANTHACEAE OF EURASIA 111
flower with a single bract, 6-merous, the petals 7. Decaisnina Tiegh.

separating to the base in anthesis; anthers dorsi-
fixed, versatile; style articulate very close to the Decaisnina Tiegh., Bull. Soc. Bot. France 42: 434, 435
base. n ¼ 9. (1895).
One sp., Cecarria obtusifolia (Merr.) Barlow,
Philippines to Queensland and the Solomon Robust plants with epicortical roots and second-
Islands. ary haustoria. Leaves mostly decussate, venation
pinnate. Inflorescences axillary, rarely terminal,
each a raceme of decussate pairs of pedunculate
5. Cyne Danser triads, each flower with a single bract. Petals 6,
rarely 5, choripetalous but basally coherent after
Cyne Danser, Bull. Jard. Bot. Buitenzorg III, 10: 291, 306 anthesis; anthers basifixed, immobile; style often
(1929).
articulate basally, stigma small, capitate. Fruit
ellipsoid, usually with persistent stylar base.
Plants with epicortical roots and secondary haus-
n ¼ 12.
toria. Leaves decussate, venation pinnate. Inflo-
Twenty-five spp., Java, Sulawesi, and Philip-
rescence a much contracted raceme of 1 or more
pines SE to Australia and the Pacific as far as the
decussate pairs of triads (rarely dyads), develop-
Marquesas.
ing below and breaking through a shell of cork,
raising a rupturing blister or calyptra as the flow-
ers expand; triads and flowers with minute ped- 8. Dendrophthoe Mart. Fig. 33
uncles and pedicels; each flower with a bract,
those of each triad forming an involucre; petals Dendrophthoe Mart., Flora 1: 109 (1830).
6, more or less choripetalous; anthers basifixed,
sessile; style often basally articulate, stigma usu- Often robust plants with epicortical roots and
ally capitate. Fruit ellipsoid, with persistent stylar secondary haustoria. Leaves alternate, scattered
base. or rarely opposite leaves; epicortical roots pres-
Six spp., the Philippines, the Moluccas, and ent. Inflorescence a simple raceme or spike
New Guinea. (rarely reduced to 2 or even a single flower),
each flower subtended by a single bract. Petals 5
(4), gamopetalous basally; mature bud usually
6. Dactyliophora Tiegh.
inflated and curved; anthers basifixed, immobile,
4-loculate; style usually with capitate stigma.
Dactyliophora Tiegh., Bull. Soc. Bot. France 41: 549
(1894). Fruit ovoid; seedling cryptocotylar. n ¼ 9.
About 38 spp., tropical Africa and S Asia to
Plants with opposite (rarely ternate) leaves and Australia.
epicortical roots bearing secondary haustoria.
Inflorescence axillary or from epicortical roots, 9. Distrianthes Danser
consisting of 1–4 whorls of triads, the whorls in
racemose order on a short common axis, triads Distrianthes Danser, Bull. Jard. Bot. Buitenzorg III, 10: 213
pedunculate, central flower sessile, lateral ones (1929), 11: 366 (1931).
pedicellate, each flower subtended by a single
bract. Petals usually 6, at anthesis distinct to the Robust plants with epicortical roots and second-
base and usually with an internal spur just above ary haustoria. Leaves decussate. Inflorescences
the inner base; anthers linear, basifixed, immo- axillary or from the epicortical roots, each an
bile, 4-locular; style articulate above the base, umbel of 2 sessile triads, the median bracts
stigma capitate. Fruit ellipsoid or ovoid. n ¼ 9. of each triad enlarged and foliaceous, enclosing
Two spp., Ceram and New Guinea, beyond its 3 flowers and connate marginally over
Malesia to Queensland and the Solomon Islands. them during development; lateral bracts small,
112 Loranthaceae
anthers basifixed, immobile; style conical basally,

stigma capitate. Fruit nearly globular; seedling
phanerocotylar.
Two spp., E India to Vietnam and W Malesia.
11. Helicanthes Danser
Helicanthes Danser, Verhand. Kon. Akad. Wetensch., Afd.

Natuurk. II, 19(6): 55 (1933).
Inflorescence reduced to a single, sessile flower,

placed at the nodes and subtended by a single
bract. Petals 5, gamopetalous, the stamens
becoming spirally twisted; anthers basifixed.
One sp., Helicanthes elasticus (Desv.) Danser,
endemic to India. See also under Genera of Africa
and Madagascar.
12. Helixanthera Lour.
Helixanthera Lour., Fl. Coch. 1: 142 (1790).
Rather large plants with epicortical roots

and secondary haustoria sometimes reaching
down along the host trunk into the earth. Leaves
decussate or scattered/crowded in false whorls.
Inflorescence a spike or raceme, each flower
with a single bract. Petals 4 or 6, choripetalous;
anthers basifixed, immobile; style simple or
Fig. 33. Loranthaceae. A–C Dendrophthoe pauciflora.
A Twig with scars of fasciculate flowers. B Flower. constricted at mid-level; stigma capitate. Fruit
C Twig. D–F D. flosculosa. D Inflorescence. E Flower. ovoid.
F Infructescence. G–I D. villosa. G Leaf. H Flower bud. About 35 spp., tropical Africa, S Asia and
I flower. J D. praelonga, inflorescence. (Danser 1931) Malesia.
narrow. Petals 6, gamopetalous; anthers basi-

13. Lampas Danser
fixed, immobile.
One sp., Distrianthes molliflora (K. Krause)
Lampas Danser, Bull. Jard. Bot. Buitenzorg III, 10: 291,
Danser, northern New Guinea. 320 (1929).
10. Elytranthe Blume Leaves verticillate, venation pinnate. Inflores-

cence axillary, each a subumbellate/subcapitate
Elytranthe Blume in Schult. & Schult.f., Syst. Veg. 7: 1611 raceme of spirally arranged, crowded triads sub-
(1830). tended by an involucre of the outermost triads;
bracts or bracteoles single under each flower.
Plants with epicortical roots and secondary haus- Petals 6, gamopetalous to above the middle;
toria. Leaves decussate. Inflorescences axillary, anthers basifixed, immobile; style articulate
each a few-flowered spike, axis decussately flat- basally, stigma capitate. Fruit unknown.
tened, each flower subtended by 3 foliaceous One sp., L. elmeri Danser; endemic to Borneo
bracts enclosing the bud. Petals 6, gamopetalous; (Sabah).
flower with a single bract/bracteole. Petals 6,

becoming S-shaped before anthesis, usually
gamopetalous to near the middle at anthesis;
anther basifixed, immobile, linear, acute, 4-locu-
late; style articulate basally, stigma small, capi-
tate. Fruit ellipsoid to globular, usually with
persistent stylar base. n ¼ 12.
About 10 spp., Malaya, Sumatra, Borneo,
Sulawesi, and the Philippines E to New Guinea.
15. Lepidaria Tiegh. Fig. 35
Lepidaria Tiegh., Bull. Soc. Bot. France 42: 439 (1895).
Stout plants with epicortical roots and secondary

haustoria. Leaves decussate. Inflorescences axil-
lary, each a more or less sessile capitulum of pairs
of monads enclosed by pairs of sterile, enlarged,
brightly colored bracts, each monad with one
bract and 2 bracteoles. Petals 6, gamopetalous;
anthers basifixed, immobile, often with small
basal spur; style conical and articulate above the
base; stigma capitate. Fruit ellipsoid to obovate.
Eight spp., endemic to N and W Malesia, with
one species reaching peninsular Thailand.
16. Loranthus Jacq.
Loranthus Jacq., Enum. Stirp. Vindob. 55, 230, t. 3 (1762),

nom. gen. cons. # 2074.
Hyphear Danser, Bull. Jard. Bot. Buitenzorg III, 10: 292,
319 (1929).
Fig. 34. Loranthaceae. A–D Lepeostegeres beccarii.
A Inflorescence in bud. B Inflorescence. C Same, longitu- Loranthus europaeus deciduous, L. odoratus ever-
dinal section. D Infructescence. E–G L. lanceifolius. green; leaves decussate to displaced. Inflores-
E Node with leaf and inflorescence, small-flowered form. cence a simple, axillary or terminal spike, with
F Inflorescence, large-flowered form. G Flower. H, I or without terminal flower; flowers sessile, singly
L. filamentosus. H Inflorescence with all flowers, except
one, taken away. I Flower. (Danser 1931) in small axial cavities, each with a minute bract,
apparently always unisexual (plants dioecious).
Petals 4 or 6, small, choripetalous; anthers basi-
fixed, immobile. Fruit nearly globular; at least
14. Lepeostegeres Blume Fig. 34
L. europaeus cryptocotylar.
Two spp., one from E Germany, Italy and SE
Lepeostegeres Blume in Schult. & Schult.f., Syst. Veg. 7 (2):
1611 (1830). Europe to S Asia and as far as Japan, the second
on Sumatra and Sulawesi; the former has no epi-
Robust, glabrous plants with epicortical roots and cortical roots, but the latter is said to have them.
secondary haustoria. Leaves mostly decussate,
venation pinnate. Inflorescences axillary, each a 17. Loxanthera Blume
pedunculate capitulum of 6–12 pairs of decussate
triads surrounded by pairs of sterile, imbricate Loxanthera Blume in Schult. & Schult.f., Syst. Veg. 7(2):
bracts; flowers 15–50, pedicellate or sessile, each 1612 (1830).
114 Loranthaceae
Fig. 36. Loranthaceae. A–C Macrosolen borneanus. A

Node with leaves and fruit. B Detached corolla with
stamens and style. C Inflorescence with calyces. D, E M.
tetragonus. D Inflorescence. E Unripe fruit. F, G M. retu-
sus. F Inflorescence with flowers in bud. G Flower, half-
opened. H, I M. tenuiflorus. H Inflorescence. I Calyx with
Fig. 35. Loranthaceae. A, B Lepidaria kingii. A Inflores- bract, prophylls and style-base. J, K M. suberosus. J Inflo-
cence. B Flower with bracteoles. C, D L. forbesii. C Inflo- rescence with flowers in bud. K Same, flowers anthetic.
rescence. D Receptacle with the outer five pairs of (Danser 1931)
involucral bracts and four unripe fruits. E L. sabaensis,
inflorescence. F, G L. bicarinata. F Inflorescence of which
the sterile and outermost fertile bracts have been taken spur; style basally articulate, stigma capitate.
away, showing three of the outermost four pairs of brac-
teoles, and the interior bracts. G Same inflorescence seen Fruit ellipsoid.
from the other side, where one longitudinal row of bracts One sp., L. speciosa Bl., Malaya, Sumatra,
has been left intact. H, I L. vaginata. H Extremity of a twig Borneo, and Java.
with two inflorescences. I Flower with bracteoles. (Danser
1931)
18. Macrosolen (Blume) Reichenb. Fig. 36
Plants with epicortical roots and secondary haus- Macrosolen (Blume) Reichenb., Repert. Herb.: 73 (1841).
toria. Leaves decussate, venation pinnate. Inflor-
escences axillary, each a raceme of decussate Robust plants with epicortical roots and second-
pairs of pedunculate triads, each flower with ary haustoria. Leaves mostly decussate. Inflores-
one bract. Petals 6, gamopetalous to above the cences axillary or from epicortical roots, each a
middle; anthers immobile, with an acute basal simple raceme or spike (rarely an umbel or
Fig. 37. Loranthaceae. Papuanthes albertisii. A–C Por-

tions of stems with inflorescences. D Flower bud. E Inflo-
rescence with young fruits, involucral bract removed.
(Barlow 1997)
Fig. 38. Loranthaceae. Sogerianthe ferruginea. A Branch-

let with inflorescences. B (One-flowered) inflorescence,
capitulum) of decussate pairs of flowers. Buds stamens and corolla fallen. S. sogerensis. C Portion of
inflated in the middle. Petals 6, gamopetalous in stem with inflorescences. D Single post-anthetic flower
and inflorescence stalk, perianth and stamens fallen. (Bar-
mature buds with 6 keels or wings at the point of low 1997, redrawn from Danser 1931 and 1939)
reflexion of the lobes; anthers basifixed, immo-
bile, linear, 4-loculate; stigma capitate. Fruit ellip-
soid to nearly globose; seedling phanerocotylar. 20. Scurrula L.
n ¼ 12.
About 30 spp., S Asia and Malesia, extending Scurrula L., Sp. Pl., ed. 1, 110 (1753).
from India to New Guinea.
Plants more or less densely covered with stellate
and dendritic hairs, with epicortical roots and
19. Papuanthes Danser Fig. 37
secondary haustoria. Leaves decussate, different
in hair cover above and below. Inflorescence
Papuanthes Danser, Bull. Jard. Bot. Buitenzorg III, 11: 360
(1931). a 3–10-flowered raceme of decussate flowers,
rarely 2-flowered; each flower with a single
Plants with epicortical roots and secondary haus- bract. Petals 4, basally gamopetalous, the floral
toria. Leaves decussate. Inflorescence a capitulum tube curved before anthesis, deeply split on inner
of (8) 12 (15) flowers in 2 rows on a common side of curve, the lobes reflexing to the opposite
peduncle and enclosed between 2 foliaceous side; anthers basifixed, immobile; style with capi-
bracts that are marginally connate during devel- tate stigma. Fruit obovoid, clavate, stipitate; seed-
opment; each flower on a short, articulated pedi- ling cryptocotylar.
cel with small bract immediately below the flower. About 20 spp., India to Taiwan and Malesia.
Petals 6, gamopetalous at anthesis to above the
middle. Anthers basifixed, immobile; stigma cap- 21. Sogerianthe Danser Fig. 38
itate. Fruit ovoid. n ¼ 9.
One sp., P. albertisii (Tiegh.) Danser, endemic Sogerianthe Danser, Verhandl. Akad. Wetensch. Amster-
to New Guinea. dam, Afd. Natuurk., 29: 106 (1933).
116 Loranthaceae
Plants with epicortical roots and secondary haus-

toria. Leaves decussate, venation pinnate but
somewhat curvinerved. Inflorescence primarily a
solitary flower on a short, articulate or rarely
non-articulate pedicel. Flowers 6-merous, gamo-
petalous, each subtended by 2 or 3 distinct or
variously united bracts; anthers basifixed, immo-
bile; stigma capitate. Fruit ovoid. n ¼ 9.
Five spp., New Guinea and Solomon Islands,
some extending to the Bismarck Archipelago.
22. Taxillus Tiegh. Fig. 39
Taxillus Tiegh., Bull. Soc. Bot. France 42: 243 (1895).
Slender to more or less robust plants with tomen-

tum of stellate hairs, with epicortical roots and
secondary haustoria. Leaves decussate. Inflores-
cence a few-flowered umbel or cluster, each
flower with a single bract. Petals 4 or 5, gamope-
talous, the floral tube curved prior to anthesis,
deeply split on the inside curve; petals reflexing
to the opposite side; anthers basifixed, immo-
bile, 4-loculate; style with capitate stigma. Fruit
ellipsoid, usually reddish, calyculus prominent.
n ¼ 9.
About 30 spp., Africa, S Asia from Sri Lanka
and Pakistan to China and the Philippines, S to
Borneo, Japan; one species in coastal Kenya.
23. Thaumasianthus Danser
Thaumasianthus Danser, Rec. Trav. Bot. Néerl. 30:

464–481 (1933).
Glabrous plants, leaves decussate, ovate; venation Fig. 39. Loranthaceae. Taxillus sericeus. A Flower-bear-
pinnate. Inflorescences at the nodes, each a ses- ing twig. B Corolla with stamens and style. (Danser 1935)
sile involucrate capitulum of 12–18 flowers
arranged in decussate triads except for the sub-
Plants glabrous to pubescent, branches terete.
terminal monads; both monads and lateral flow-
Leaves alternate or decussate, venation pinnate.
ers of triads with 2 bracteoles each, median
Inflorescence a sessile or pedunculate head of <6
flowers of triads clasped in 3 bracts each; petals
sessile flowers connate with the involucre of 3–6
6, gamopetalous; anthers linear, acute, basifixed,
basally connivent, foliaceous bracts representing
immobile; stigma capitate. Fruit unknown.
the primary bracts of each flower. Flowers bisex-
One sp., T. amplifolia (Merr.) Danser,
ual, petals 5; filaments distinct, erect above the
endemic to the Philippines.
corolla tube; anthers linear, sub-dorsifixed,
immobile, style filiform, stigma small. Fruit
24. Tolypanthus (Blume) Reichenb. obovate-oblong.
One rare, endemic sp. in SW Sri Lanka; about
Tolypanthus (Blume) Reichenb., Repert. Herb.: 73 (1841). 3 others in continental SE Asia.
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young haustorial gland in Comandra (Santalaceae). Zaki, M., Kuijt, J. 1994. Ultrastructural studies on the
Can. J. Bot. 54: 2315–2327. embryo sac of Viscum minimum. II. Megagameto-
Treub, M. 1881. Observations sur les Loranthacées. Ann. genesis. Can. J. Bot. 72: 1613–1628.
Jard. Bot. Buitenzorg 2(1): 54–76. Zaki, M., Kuijt, J. 1995. Ultrastructural studies on the
Venturelli, M. 1981. Embriologia de Struthanthus vulgaris embryo sac of Viscum minimum. I. Megasporogene-
(Loranthaceae-Loranthoideae). Kurtziana 14: 73–100. sis. Protoplasma 185: 93–105.
Venturelli, M. 1983. Estudos embriológicos em Lorantha-
ceae: gênero Tripodanthus. Kurtziana 16: 71–90.
Misodendraceae
Misodendraceae J. G. Agardh (1858), nom. fam. cons.; Orfila, Misodendraceae de la Argentina y Chile.
Fundación Elias y Ethel Malamud, Serie Cientı́fica, pp. 1–73 (1978); Rossow, Parodiana 1: 245–270 (1982), rev.; Zavero
et al., Fontqueria 48: 225–239 (1997), cladistics.
Relatively small parasitic plants on the branches of tics of the unisexual flowers and inflorescences as
trees (nearly exclusively Nothofagus spp.), gla- well as the post-floral extension in the minute
brous or with sparse, short, unicellular epidermal fruits of staminal remnants into long feathery
hairs. Stems stout and smooth or slender and with organs that serve as aids to dissemination.
tuberculate surface; branch tips aborting, branch-
ing sympodial, the ramifications bearing inflores- ANATOMY. The verrucose stem surface of some spe-
cences only in the second year. Leaves alternate, cies of Misodendrum is caused by wart-like raised
thin and deciduous or squamate and permanent; portions bearing a stoma each of which has a large,
prophylls absent. Plants dioecious or monoecious. expanded substomatal cavity below. The lateral
Flowers unisexual (very rarely bisexual) and lack- buds of thick-stemmed species like M. brachysta-
ing obvious perianth members. Inflorescences chum are initially buried by what appears to be
spike-like or racemose, subtended by a petiolate, secondary cortical tissue, the emerging shoot or
foliar bract, or along that petiole, or sessile in small inflorescence thus of seemingly endogenous origin
clusters in the axil of a sessile foliar bract. Stami- and leaving a basal crater-like rim.
nate flowers consisting of 2 or 3 monothecal Misodendraceae wood shows numerous pecu-
stamens attached around a central, often lobed liarities (Metcalfe and Chalk 1950; Carlquist 1985).
cushion, stamens with distinct filaments or each In some species (subgenus Angelopogon), the vas-
stamen reduced to a sessile anther; anthers initially cular cambium is essentially inactive in ray areas.
bilocular, dehiscing with a transverse, terminal Thus the stem vascular tissues are without a con-
slit. Pollen spheroidal, short-spinulate, with 4–12 tinuous wood cylinder, the bundles increasing
apertures distributed over the surface. Pistillate radially but separated by permanent medullary
flowers sessile, reduced to an ovary with 3 linear rays; there may be one or two interrupted cylin-
stigmatic surfaces, the ovary wall with three con- ders of clustered cortical, thick-walled sclereids
spicuous longitudinal grooves each containing an and sometimes a similar series just internal to
embryonic seta; each seta eventually elongating to the protoxylem. A second circle of vascular bun-
become a long, feather-like structure the tip of dles forms in the pith in subgenus Misodendrum.
which may be straight and acute or recurved and Rays consist entirely of fibers or thin-walled cells.
blunt. Fruit a one-seeded achene attached to the In subgenus Misodendrum, however, there is an
three long setae. n ¼ 8. active cambium both in fascicular and interfasci-
A single genus, Misodendrum, with about 8 spe- cular areas. Vessel elements are extremely short
cies, restricted to southern South America from and narrow and have simple perforations. There
Tierra del Fuego northwards to Nahuel Huapi appear to be some structural differences between
National Park on the Argentine side and reaching subgenus Angelopogon and subgenus Misoden-
Prov. Maule (35 S) on the Chilean side. drum in vessel pitting. Except for some unique
Misodendraceae form a sharply distinct family features, wood anatomy appears to be similar to
of ramal parasites defined by unique characteris- that in Loranthaceae.
122 Misodendraceae
B R A N C H I N G P A T T E R N S . In probably all species

of Misodendrum, shoots abort at the apex. In
leafy species such as M. oblongifolium and
M. brachystachyum, there are two entirely differ-
ent branch types (Fig. 40). Inflorescence-bearing
shoots are produced near the tip of older shoots
and bear broadly lanceolate, acute-tipped leaves,
the upper ones associated with inflorescences.
The entire shoot is dropped after flowering or
fruiting. Just below such shoots, purely vegetative
innovations bearing much elongated, narrow,
round-tipped leaves emerge; their distal portions
will repeat the pattern in the following growing
season, when the shoot is leafless. In squamate
species like M. punctulatum, all innovations are
eventually reproductive, with inflorescences in
axillary portions to most scale-leaves during the
second growing season. The exact branching pat-
tern of some species, like M. recurvum, has not
been adequately elucidated.
T H E H A U S T O R I U M . In most species, the attach-

ment is a very simple one in that the endophyte
remains strictly localized (Fig. 41A). This calls
forth a cup-like structure from the host, somewhat
like a small woodrose but with a relatively smooth
host-parasite interface. However, I have observed
sprouting from the endophyte in a squamate spe-
cies (probably M. punctulatum) near Ushuaia,
Argentina, and this can only mean that the endo-
phyte of that species is fragmented.
I N F L O R E S C E N C E . Inflorescences are spike-like or

racemose, the flowers subtended in solitary or
paired fashion by a bract or forming an axillary
raceme; sometimes the base of the latter is partially
connate with the base of the foliaceous bract.
F L O W E R S (Fig. 41). Pistillate flowers are always

sessile, consisting mostly of a narrowly ovoid Fig. 40 Misodendraceae, branching patterns: A Misoden-
drum punctulatum. B M. oblongifolium. Note the differences
ovary on which three separate perianth members in position of flowers, and the development of branches
are connate with the ovary for their full length, from sleeping buds (asterisks) in B. (Kuijt 1969, drawn by
their distinct lateral wings leaving narrow slits author)
between them from which, at anthesis, three
small bristle-like staminodial setae emerge. A
prominent, 3-parted, nearly sessile stigma crowns reaches far into the column, ramifying apically.
the pistillate flower. The ovarian cavity is simple, The staminate flower is stalked, apetalous, con-
a placental column arising from the base bearing sisting of two or three at least initially biloculate
three pendent, reduced ovules which lack integu- anthers with terminal slits, sessile or on well-
ments. A long, tubular haustorium is formed by developed filaments arranged around a central
the antipodal cells of the three embryo sacs and cushion. Following anthesis, the setae of the
Misodendraceae 123
P O L L E N . The structure of pollen is essentially

uniform across the genus, not suggesting any
infrageneric division and only vaguely suggesting
affinities to other families (Feuer 1981). Grains are
subspheroidal, sparsely echinate, and polyporate,
the number of circular pores ranging from 3–19,
scattered randomly over the surface. Palynologi-
cally, no clear affinities emerge except a possibly
remote one to Eremolepidaceae.
P O L L I N A T I O N . Misodendrum flowers are

probably entomophilous, possibly pollinated by
beetles of the family Cantharidae, but some wind-
pollination cannot be excluded, especially consid-
ering the local stormy climate.
F R U I T A N D S E E D . The fruit is a minute, wind-

dispersed achene, becoming entangled in the
branches of surrounding trees (Fig. 41). The seed-
ling is said to have two cotyledons that are nearly
completely connate in tube-like fashion, the radic-
ular pole forming a disk that is applied to the host
surface and from the ventral surface of which the
endophyte emerges. It is not clear how the radicu-
lar pole reaches the host surface. The endosperm
contains chlorophyll.
P H Y L O G E N Y . Misodendraceae have frequently

been traced back to ancestral Santalaceae, but
the fact that (sterile) stamens alternate with the
perianth segments, and the fact that the ovary is
essentially superior, would seem to indicate an
Fig. 41 Misodendraceae. A Misodendrum brachysta- origin from early Olacaceae, the only other San-
chyum, old haustorium showing cuplike woodrose of host. talalean family in which such conditions exist.
B M. punctulatum. Staminate flower with bract. C M. bra- The recent revised classification of Santalales by
chystachyum, pistillate flower with emerging setae.
D M. linearifolium, apex of seta. E M. oblongifolium, fruit. Nickrent et al. (2010) places Misodendraceae
F Same, enlarged. G M. brachystachyum, seed germinating close to Schoepfiaceae, itself a very heterogeneous
on Nothofagus antarctica. (All from Kuijt 1969, drawn by family having structurally little in common with
author, A, B, C and G redrawn from Hooker 1846)
Misodendraceae. Zavaro et al. (1997), in a cladis-
tic study based on structural features, considered
pistillate flower elongate to become long, feather- the family a sister group of Eremolepidaceae.
like organs reaching 10–85 mm in length and It is notable, considering the near-restriction
covered by innumerable uniseriate trichomes, in to Nothofagus as hosts, that the Nothofagus forests
some species the setae with a hooked tip. These in the Old World lack Misodendraceae. The wind
organs are considered to be modified stamens dissemination of the family, unique in the order,
that thus alternate with the 3 perianth segments; points to a local origin in its present location,
in consequence, the ovary is to be regarded as where stormy weather is notorious all through
superior. the year.
124 Misodendraceae
Misodendraceae as a family are stated to be what appear to be significant differences in anato-

some 75 million years old. mical stem structure.
Only one genus:
Misodendrum Banks ex DC. Figs. 40, 41 References

Misodendrum Banks ex DC., Prodr. 4: 285 (1830). Carlquist, S. 1985. Wood and stem anatomy of Misoden-
Myzodendron Banks et Sol. ex R. Br. (1844). draceae: systematic and ecological conclusions.
Brittonia 37: 58–75.
Feuer, S. 1981. Pollen morphology and relationships of
References and description as those given for the the Misodendraceae (Santalales). Nordic J. Bot. 1:
family above. 731–734.
Two subgenera have been recognized in the Hooker, J.D. 1846. Flora Antarct. 2: 239–302. London:
Reeve, Brothers.
past, subg. Misodendrum (including the illegiti- Kuijt, J. 1969. The biology of parasitic flowering plants.
mate subgenus Gymnophyton Hook. f., which Berkeley and Los Angeles: Univ. Calif. Press.
contains the type species of the genus) and subg. Metcalfe, C.R., Chalk, L. 1950. Anatomy of the dicotyle-
Angelopogon (Tiegh.) Rossow, the latter based on dons. Oxford: Clarendon Press.
the genus Angelopogon Tiegh. Palynological fea- 2010. A revised classification of Santalales. Taxon
tures do not support such a subgeneric separation 59: 538–558.
(Feuer 1981), and Skottsberg earlier (1935) spoke Skottsberg, C. 1935. Myzodendraceae. In: Engler, A., Prantl,
of structural continuity between the two subge- K., Die nat. Pflanzenfam., 2nd edn, 16b: 92–97.
Zavaro CA, Crisci JV, Morrone JJ. 1997 Synopsis and
nera, and felt that the two subgenera are of dubi- cladistics of the genus Misodendrum (Misodendra-
ous value. Carlquist (1985), however, showed ceae, Santalales). Fontqueria 48: 225–239
Octoknemaceae
Octoknemaceae Tiegh. in C.K. Schneider, Just’s Bot.
Jahresber. 33: 519 (1907), nom. fam. cons.
Shrubs or trees to 30 m high; not documented to sepals or a calyculus. All species are dioecious,
be parasitic. Young twigs glabrous to densely flowers bearing sterile organs of the opposite sex;
pubescent, all other growth with stellate or the style is massive and short, terminating in a
semi-dendritic hairs, including inflorescences strikingly lobed, flat stigma, and the endosperm
and flowers; indumentum scale-like in Octo- is deeply grooved. The family continues to be
knema affinis. Leaves alternate, entire, estipulate, enigmatic, but recent molecular work (Nickrent
petiolate; stomata on abaxial surface only. Dioe- et al. 2010) has solidified its position within San-
cious. Inflorescences axillary, solitary; flowers talales. The molecular and morphological work
pentamerous (trimerous in one species), sepals by Malécot et al. (2004) indicated that the genus
reduced or absent. Staminate inflorescence race- was a basal member of the basal-most clade of
mose, sometimes branched, the flowers with Olacaceae, whereas Nickrent et al. (2010) pre-
apparently epipetalous or distinct stamens, ferred to keep Octoknemaceae separate. A recent,
anthers dorsibasifixed, bilocular, reduced style detailed monograph of Octoknema (Gosline and
present. Female inflorescence spicate; pistillate Malécot 2012) seems to leave the matter open
flowers with (3)5 small staminodia; ovary infe- once again. Plants of the genus are especially
rior, 3-chambered below through thin separa- reminiscent of Coulaceae like Minquartia, shar-
tions that soon collapse; ovules 3, unitegmic or ing inflorescence and (superior) ovary structure,
bitegmic, pendent from the tip of a central funic- stellate hairs, and venation pattern. The stigmatic
ulus; style massive, stigma with 3–5 conspicuous, surfaces of Coulaceae, however, do not have the
flat, often notched, spreading lobes. Fruit dark striking, flat and spreading lobes seen in pistillate
green, yellow, orange or bright red, with (at matu- Octoknema flowers. The dioecy of Octoknema
rity) soft parenchymatous surface tissue below does not occur in Coulaceae, nor does the dis-
which is a layer of sclerenchyma. Seed solitary, tinctly furrowed seed.
with 6 or 9–11 longitudinal grooves reaching into No demonstration of parasitism in Octokne-
the endosperm; embryo with massive radicular maceae exists but Nickrent et al. (2010), basing
pole, with 2(6) flat cotyledons, germination pha- their views on the position of the family in a
nerocotylous, epigaeous. molecularly based consensus phylogeny, suggest
A unigeneric family with at least 14 spp. in that it may be semiparasitic. The anatomical
western and central equatorial Africa and one structure of leaves and wood indicate a degree
outlier in the eastern arc mountains (Gosline of isolation from Olacaceae (Baas et al. 1982; Van
and Malécot 2012). den Oever 1984), while pollen structure suggests a
Octoknemaceae are sharply circumscribed position near Opiliaceae (Lobreau-Callen 1982).
and characterized by stellate or semi-dendritic The genus has also been placed in subfamily
epidermal hairs at least on inflorescences and Schoepfioideae of Olacaceae (Schultze-Motel
flowers, an inferior ovary and mostly the lack of 1964). A detailed description of wood and leaf
126 Octoknemaceae
anatomy, pollen structure, and phytochemistry is Octoknema Pierre, Bull. Soc. Linn. Paris 2: 1290
provided by Gosline and Malécot (2012). (1897); Gosline & Malécot, Kew Bull. 66: 367–404
The suggestion made by Nickrent et al. (2010, (2012), rev.
pp. 541–543) that Octoknemaceae might be Description as for the family.
joined with Erythropalaceae is not here regarded
as a reasonable one, partly in the face of their
already unacceptable inclusion of Maburea and References
Heisteria in that family.
Only one genus: Baas, P., Van Oosterhoud, E., Scholtes, C.J.L. 1982. Leaf
anatomy and classification of the Olacaceae, Octo-
Octoknema Pierre Fig. 42 knema, and Erythropalum. Allertonia 3: 155–210.
Gosline, G., Malécot, V. 2012. A monograph of Octoknema
(Octoknemaceae-Olacaceae s.l.). Kew Bull. 66:
367–404.
Lobreau-Callen, D. 1982. Structure et affinités polliniques
des Cardiopterygaceae, Dipentodontaceae, Erythro-
palacaeae et Octoknemataceae. Bot. Jahrb. Syst. 103:
371–412.
Louis, J., Léonard, J. 1948. Octoknemaceae. In: Flore de
Congo Belgique et du Ruanda-Urundi, Vol. 1. Brux-
elles: INÉAC.
Malécot, V., Nickrent, D.L., Baas, P., Van den Oever, L.,
Lobreau-Callen, D. 2004. A morphological cladistic
analysis of Olacaceae. Syst. Bot. 29: 569–586.
59: 538–558.
Schultze-Motel, W. 1964. Reihe Santalales. In: Melchior,
H. (ed.) Engler’s Syllabus der Pflanzenfamilien. Ber-
lin: Borntraeger.
Van den Oever, I. 1984. Comparative wood anatomy of
the Olacaceae. In: Sudo, S. (ed.) Proc. Pacific
Regional Wood Anatomy Conference, Tsukuba.
Fig. 42. Octoknemaceae. Octoknema affinis. A Branch

with staminate flowers. B Branchlet with pistillate flowers.
C Staminate flower bud. D, E Staminate flowers. F Pistil-
late flower bud. G, H Pistillate flowers. I Fruit. J Same,
transverse section. K Seed. (Louis and Léonard 1948,
drawn by J.M. Lerinckx)
Olacaceae
Olacaceae R. Br. (1818), nom. cons., emend. Nickrent et al. (2010); Schellenberg, Festschrift,
Deut. Bot. Gesellsch. 50a: 136–145 (1932); Sleumer, Blumea 26: 145–168 (1980); Sleumer,
Fl. Males. I, 10: 1–29 (1984); Sleumer, Fl. Neotropica 38: 1–159 (1984); Malécot et al., Syst.
Bot. 29: 569–586 (2004).
Trees or shrubs, at least some known to be semi- doubt in modern work. Relationships to Icacinaceae
parasitic. Leaves alternate, petiolate, estipulate, and Erythropalaceae, as initially suggested by
venation pinnate, often conspicuous. Inflorescence Bentham and Hooker (1862–1883), have not been
an axillary, few-flowered raceme or spike or umbel, substantiated except that Nickrent et al. (2010)
flowers rarely solitary or clustered at the nodes placed Heisteria and Maburea in Erythropalaceae
without common axis. Flowers bisexual, distylous (see comments below). The latter authors excluded
in Dulacia and Ptychopetalum, pedicellate (more Brachynema from Olacaceae, a genus here included.
or less sessile in inflorescence depressions in The classical treatment of Sleumer (1935)
Strombosiopsis). Calyculus small to moderate, presented the following internal organization of
sometimes accrescent in fruit; petals 4–6, distinct Olacaceae:
or basally united. Stamens basally epipetalous, as
many as the petals and opposite them, or twice as Subfam. Dysolacoideae Engler, Nat. Pflanzenfam.,
many and also alternating, filaments present; Nachtr. 149 (1897)
anthers basifixed, longitudinally dehiscent, some- Tribe Couleae Engler (1897): Coula, Ochanostachys,
times with terminal, acute connective. In Olax, Eganthus, Endusa, Minquartia
variable numbers of stamens are staminodial, Tribe Heisterieae Engler (1897): Heisteria, Chauno-
their sterile anthers deeply forked. Tetrastylidium chiton
with glandular disk surrounding the ovary. Ovary Tribe Anacoloseae Engler (1897): Brachynema,
mostly superior, (semi-) inferior in Dulacia, Strombosiopsis, Tetrastylidium,
Scorodocarpus, Strombosia, and Strombosiopsis, Scorodocarpus, Cathedra, Anacolosa, Strombosia,
with 2 or 3 locules below becoming one locule Worcesterianthus
above. Fruit a 1-seeded drupe. Endosperm copious, Tribe Ximenieae Engler (1897): Ximenia
starchy, the calyculus in some strongly accrescent Subfam. Olacoideae Engler (1897)
and surrounding the fruit or (Heisteria) forming a Tribe Olaceae Engler (1897): Ptychopetalum, Olax,
deeply lobed, loose, brightly colored cup. Liriosma
Olacaceae, here treated as comprising 13 Tribe Aptandreae Engler (1897): Aptandra, Ongo-
genera, are an essentially pantropical family, kea, Harmandia
represented more or less equally in tropical Subfam. Schoepfioideae Engler (1897): Schoepfia
America, Africa, and Asia. Unlike the situation
in the related Loranthaceae, several genera occur
Nickrent et al. (2010) recognized the follow-
in two or all three of these areas.
ing families and genera:
The circumscription of Olacaceae has varied
widely over the years from its initial formulation Erythropalaceae: Erythropalum, Heisteria, Maburea
in 1836 to the recent study by Nickrent et al. (2010), Strombosiaceae: Engomegoma, Scorodocarpus,
but its affinity to Santalaceae and, beyond that Strombosia, Strombosiopsis, Tetrastylidium
family, to Loranthaceae, has scarcely been in Coulaceae: Coula, Minquartia, Ochanostachys
128 Olacaceae
Ximeniaceae: Curupira, Douradoa, Malania, including the common cristarque cells. Brachy-
Ximenia to astrosclereids are widespread in the family, as
Aptandraceae: Anacolosa, Aptandra, Cathedra, are columnar sclereids in several genera, and
Chaunochiton, Harmandia, Ongokea, Phanerodis- fibrous to filiform fibers are seen in some but
cus, Hondurodendron not all species of some genera. Heisteria is
Olacaceae: Dulacia, Olax, Ptychopetalum unusual in having scalariform perforation plates
Octoknemaceae: Octoknema in its vessel members, while other genera, as far as
Schoepfiaceae: Arjona, Quinchamalium, Schoepfia is known, have simple perforation plates. The
genus also has conspicuous laticifers in its leaves.
The molecular studies of Malécot et al. (2004) Leaf anatomy generally supports the view that
and Nickrent et al. (2010) have provided a radical Olacaceae constitute the basal family within San-
reorganization that gave, in addition to a revised talales.
Olacaceae, the families Aptandraceae, Coulaceae,
Erythropalaceae, Schoepfiaceae, Strombosiaceae, INFLORESCENCE. The inflorescence of Olacaceae var-
and Ximeniaceae. In the present treatment, Ery- ies from a simple or branched spike, sometimes
thropalaceae (Erythropalum) are excluded from greatly condensed, to axillary clusters of flowers
Santalales. I have found it impossible to separate or few-flowered racemes/umbels; in some cases,
Strombosiaceae from Olacaceae, and the two are the flowers are individually axillary, and we can-
united here. The other families, however, are not speak of inflorescences.
accommodated in my treatment. Nickrent et al.
(2010), because of weak support for a sister rela- FLORAL STRUCTURE. The flowers of Olacaceae are
tionship with Erythropalaceae, entertained the mostly bisexual, and have a weakly developed
idea of joining Strombosiaceae with them, but calyculus that, in some cases, expands greatly in
that appears to be a problematic position, also fruit. The 4–6 petals are basally joined especially
considering the fact that Maburea and Heisteria in Brachynema, where they form a floral tube.
are there part of Erythropalaceae (they are here The anthers are as many as the petals and oppo-
included in Olacaceae). Nevertheless, it can be site them, or double that number; the variable
seen that, except for changes in ranks, the recog- abortion of stamens in Olax is described in that
nition of Sleumer’s suprageneric taxa essentially genus. Anthers are ovoid to elongate, mostly
prevails except for Tribe Anacoloseae. dithecal. The ovary is usually superior, the lower
portion of the ovarian cavity partitioned in 2–5
MORPHOLOGY. The young leaves and twigs of Ola- compartments, one elongate ovule suspended in
caceae are sometimes somewhat pubescent when each; the integuments are one or two, or none.
young, becoming glabrous. As in nearly all other
members of the order, leaves are estipulate, EMBRYOLOGY. A detailed study is available for the
entire, and provided with a petiole; phyllotaxy is ovary and embryology of Olax (Agarwal 1963).
alternate, and venation is pinnate and usually The upper portion of the ovarian cavity is uniloc-
evident. ular, but its lower portion is 3-lobed. A central
funiculus extends from the base of the cavity to
VEGETATIVE ANATOMY. Wood and leaf anatomy of the top, three ovules being suspended from its
Olacaceae have been exhaustively detailed by apex, turning upwards when the megaspore
Reed (1955) and Baas et al. (1982), respectively, mother cells and single integuments differentiate.
but are difficult to summarize because of the In each ovule, the female gametophyte elongates
extensive diversity in each case as well as the greatly in both directions, and in two species a
different genera included in those studies. Leaf lateral caecum develops that grows into the base
anatomy, especially, shows much variation from of the funiculus. The mature embryo sac of Olax
genus to genus, and sometimes within a genus. wightiana grows into the top of the ovarian cavity;
Paracytic stomata, with one or two pairs of sub- it remains within the ovule in O. stricta. An aggres-
sidiary cells, are common in Olacaceae, and are sive, multinucleate endosperm haustorium grows
regarded as an ancestral feature. As in most deeply into the base of the ovarian tissues, where it
woody dicotyledons, they are usually limited to may branch profusely. Both major embryo sac
abaxial surfaces. Crystals of various types occur, developmental types occur in the genus Olax
KEY TO THE GENERA OF OLACACEAE 129
(Polygonum type in O. scandens and O. stricta; retained here; I follow Sleumer (1935) in excluding
Allium type in O. wightiana). Erythropalaceae from Santalales.
POLLEN MORPHOLOGY. The genera that Sleumer

KEY TO THE GENERA OF OLACACEAE
(1984b) included in Olacaceae were according to
him clearly separable into two groups on the basis
1. Leaf very shallowly lobed, the secondary veins
of aperture morphology. Tricolpate pollen charac-
confluent with the margin; corolla mostly tubu-
terizes Scorodocarpus, Strombosia, Strombosiopsis,
lar, transversely striped; petal lobes with hairy
and Tetrastylidium, while 6-diploporate pollen is
median streak 2. Brachynema
found in Anacolosa, Cathedra, and Phanerodiscus
– Leaves not lobed, secondary veins not confluent
(the latter also in the African Ptychopetalum, while
with margin; petals distinct or basally coherent,
its South America species are predominately tripo-
neither forming a tube nor transversely striped;
rate; Feuer 1978). There is much infraspecific varia-
petals lacking hairy median streak 2
bility in pore number in all the above genera. Pollen
2. Flowers distylous 3
of several African genera of Olacaceae is described
– Flowers not distylous 4
and illustrated in Lobreau-Callen (1980) and Bon-
3. Fertile stamens 3; staminodia 6, deeply bifid,
neville et al. (1982).
both stamens and staminodia with hairy fila-
ments; ovary semi-inferior 4. Dulacia
POLLINATION. There appears to be no published
– All (or most) stamens fertile, filaments glabrous;
account of pollination in Olacaceae.
ovary superior 9. Ptychopetalum
4. Flowers sessile, crowded on thick inflorescence
FRUIT, SEED, DISPERSAL, AND THE SEEDLING. The
axis, in small individual depressions and each
nature of Olacacean fruits strongly suggests ani-
subtended by a small bract and two prophyllar
mal dispersal.
bracteoles; anthers with narrowly triangular
Reed (1955) reports 2 or 3 cotyledons (See
connectival horn 12. Strombosiopsis
main introduction).
– Flowers sessile or pedicellate, not in individual
depressions; floral bracts and prophyllar brac-
THE ENDOPHYTE. The structure of the endophyte in
teoles absent; anthers lacking connectival horn 5
Olacaceae was described in the early account of
5. Stamens 8 or more, including staminodia, if any
Olax by Barber (1907), and extended in a study of
6
graniferous tracheary elements (Fineran et al.
– Stamens 6 or fewer (see also Olax sect. Estami-
1987) and a focus on the haustorial interface
nodiales) 9
(Kuo et al. 1989). It forms a relatively simple
6. Both stamens and staminodia present 8. Olax
wedge extending to, and partly embedded into,
– Staminodia absent (see also Olax sect. Estami-
the host xylem, with scattered xylem-xylem con-
nodiales) 7
nections greatly outnumbered by parenchyma
7. Leaf laticifers present; calyx much enlarged in
contacts. For early developments prior to host
fruit 6. Heisteria
entry, see the introduction to the present order.
– Leaf laticifers absent; calyx not accrescent 8
8. Venation pinnate; anthers linear; ovary inferior
SYSTEMATICS. The genera Maburea and Heisteria
or semi-inferior; Indonesian area
were placed by Nickrent et al. (2010) in the family
10. Scorodocarpus
Erythropalaceae, the curious genus Erythropalum
– Venation palmate (4 large basal secondary
being monotypic. It is a scandent, tendril-bearing
veins); anthers not linear; ovary superior;
liana from Indomalaysia with a slender, com-
South America 7. Maburea
pound dichasial inflorescence (see Kuijt 1969, his
9. South America 10
Figs. 3–17), and inclusion of the three genera in
– Paleotropical 11
one family is nothing short of incongruous. It
10. Petals 4; anthers broadly lanceolate, nearly
should be noted that Maburea was originally
without filaments, transversely septate
placed in Olacaceae, and that very few, if any,
13. Tetrastylidium
previous workers have doubted the position of
– Petals 5 or 6; anthers not as above 3. Cathedra
Heisteria in the same family. Both genera are
130 Olacaceae
11. Adaxial petal surface with dense, elongated

papillar hairs; fruiting stalk elongating to
2–3.5 cm 5. Engomegoma
– Adaxial petal surface not papillate; fruiting stalk
scarcely elongating 12
12. Petals 5, not concave below; anthers glabrous
11. Strombosia
– Petals 6; anthers bearded, placed in concave
lower portion of petals 1. Anacolosa
GENERA OF OLACACAEAE
1. Anacolosa (Blume) Blume Fig. 43
Anacolosa (Blume) Blume, Ann. Mus. Bot. Lugd.

Bat. 1: 250, t. 46 (1850).
Shrubs with alternate, coriaceous, entire leaves.

Flowers very small, pedicellate, bisexual, crowded
in leaf axils; calyx small, cupulate, weakly 6-
toothed; petals 6, thick, concave below, where
containing the stamens, above bearded and with
triangular apex; stamens 6, epipetalous, filaments
flat; anthers with terminal, brush-like tuft of Fig. 43 Olacaceae. Anacolosa frutescens. A Flowering branch.
hairs; glandular disk united with ovary, enlarging B Flower bud. C Flower, front part of calyx and some petals
removed. D Petal inside. E Anther, front side (left), and back.
during fruit development; ovary with a single F Fruits. (Sleumer 1984a, drawn by J. van Os)
locule or incompletely partitioned, bearing a cen-
tral, distinct funiculus with 3 pendent ovules;
style conical. Fruit a drupe, with hard inner cas- margin very shallowly lobed, with glandular
ing, containing a single seed; cotyledons 2. teeth; secondary veins confluent with leaf margin.
About 22 spp., mostly in tropical Asia, from Flowers bisexual; calyx cupulate, at first weakly 5-
India to the Philippines and Solomon Islands, one lobed, enlarging after anthesis; corolla with long,
sp. in Madagascar, and one in NE Australia (Cape transversely banded tube and 5 lanceolate, dis-
York Peninsula). tinct limbs that bear a hairy median streak;
Anacolosa was placed in Olacaceae tribe Ana- stamens 5, basally connate with the corolla, fila-
coloseae by Sleumer (1935), but included in ments short, anthers with longitudinally dehisc-
Aptandraceae by Nickrent et al. (2010). Since it ing anthers and elongated, thread-like
lacks the critical androecial features of that fam- connective; pollen porate; ovary with accrescent
ily, I here follow Sleumer and others in restoring calyculus that forms a cup under the fruit, sessile,
it to Olacaceae. with 4 or 5 basal recesses each with an ovule
hanging from the top of the partition; stigma
2. Brachynema Benth. Fig. 44 nearly sessile. Fruit globose, covered with a hard
pericarp, containing a single, longitudinally
Brachynema Benth., Transact. Linn. Soc. 2: 125, t. 22 grooved seed.
(1859); Sleumer, Flora Neotrop. 38: 99–102 (1984). One sp., Brachynema ramiflorum Benth.,
northern Brazil and Amazonian area.
Trees with alternate, ovate-oblong, petiolate Brachynema is a rare, curious genus that
leaves, the petioles pulvinate at both ends, remains of controversial standing. Sleumer
young growth with sparse unicellular hairs; leaf (1935) accepted it as belonging to Olacaceae, but
GENERA OF OLACACAEAE 131
known about the chemistry of Brachynema. On

balance, therefore, it seems best to accept Brachy-
nema in the present position.
3. Cathedra Miers Fig. 45
Cathedra Miers, Ann. Mag. Nat. Hist. II, 7: 452, 457

(1851); Sleumer, Fl. Neotrop. 38: 106–111 (1984).
Trees with reddish bark, leaves coriaceous,

short-petiolate. Flowers crowded in small clusters,
bisexual, pedicellate; calyx fleshy, cupulate, short-
hairy, weakly 5/6 toothed, not or hardly enlarged
in fruit; petals 5 or 6(7), distinct, fleshy, triangular,
elongate, hairy in the middle, placed on a fleshy,
disk, with basal cavity accommodating the
stamens; stamens 5 or 6, opposite the petals and
half as long, epipetalous, with very short, flat fila-
ments and nearly quadrangular anthers; glandular
disk fleshy, as long as the calyx or nearly so; ovary
superior, conical, 2-loculate below, with 2 pendent
ovules; style short, with 3-lobed stigma. Fruit a
drupe with thin exocarp and hard endocarp,
enclosed by the enlarged, cupulate disk and
occasionally by an enlarged prophyll.
Fig. 44 Olacaceae. Brachynema ramiflorum. A Twig. B Five spp., tropical South America.
Inflorescence. C Flower. D Corolla cut open. E Ovary, Like Anacolosa, Cathedra was included in
longitudinal section. F Enlarged calyx and fruit. G Seed. Olacaceae tribe Anacoloseae by Sleumer (1935),
(Sleumer 1984b)
but placed in Aptandraceae by Nickrent et al.
(2010). Lacking the curious androecial modifica-
the recent treatments by Malécot et al. (2004) and tions of that family, it seems more appropriate to
Nickrent et al. (2010) excluded it from the order, keep it in Olacaceae.
the former suggesting an unspecified placement
in Ericales. Unfortunately, the crucial work on the 4. Dulacia Vell. Fig. 46
ovule characteristics and embryology of Brachy-
nema that would be necessary with regard to a Dulacia Vell., Fl. Flumin. 1: t. 78 (1825); Sleumer, Fl.
comparison to Ericales has not been done. There Neotrop. 38: 116–131 (1984).
are significant anatomical details, however, that
allow at least a provisional present placement Trees or shrubs with thin, yellow branches; leaves
here. Baas (in Maas et al. 1992) writes that “In lanceoate to ovate, alternate, entire. Inflorescence
almost all leaf anatomical characteristics, a raceme or panicle. Flowers distylous, with small
Maburea resembles Brachynema”, the differences calyculus that enlarges and almost completely
being of minor importance, and Van den Oever encloses the fruit at maturity; petals 6, coherent
(unpublished; cited in Maas et al. 1992) compares to their middle, fertile stamens 3, with flat, pilose
its wood anatomy to Heisteria; in both cases, filaments; staminodia spatulate, 6, with deeply
vessel members have scalariform perforation forked tip; ovary semi-inferior, densely pilose,
plates. Pollen structure links Brachynema to sev- 3-loculate below, with 3 ovules pendent from a
eral other genera of the order (Feuer 1977; central funiculus; style nearly as long as the
Lobreau-Callen in Maas et al. 1992). Nothing is petals, stigma small, 3-lobed. Fruit ellipsoid,
132 Olacaceae
Fig. 45 Olacaceae. Cathedra rubricaulis. A Habit. B

Branchlet with fruit. C Flower bud. D Petal and stamen.
E Flower, longitudinally sectioned. (Sleumer 1984b)
1-seeded, the enveloping calyx fleshy, exocarp Fig. 46 Olacaceae. Dulacia candida. A Flowering branch.
hard; seedling, dicotylous? B Portion of flower showing one stamen and two stami-
nodes. C, D Dolichostylous flower. E Pistil and two
About 14 spp., tropical South America. stamens of brachystylous flower. F Drupes. G Upper
part of drupe with hairy top of ovary. (Sleumer 1984b)
5. Engomegoma Breteler
Engomegoma Breteler, Bot. Jahrb. Syst. 118: pollen mostly isopolar, ca. spherical, nearly trian-
114–117 (1996). gular in equatorial outline, tricolpate; ovary supe-
rior, broadly conical, stigmatic lobes 3 or 4,
Tall trees to 35 m, glabrous, not known to be locules 3 or 4, each with one pendulous ovule.
parasitic. Leaves alternate, coriaceous, with dis- Fruit with stalk 2–3.5 cm long, not known at
tinct petiole 7–17 mm long, blade ovate-elliptic, maturity.
7–18 x 3–8 cm, apex obtusely acuminate, base One sp., Engomegoma gordoni Breteler,
obtuse; venation obscure, pinnate, with 5–8 Gabon.
main laterals, midrib flat or nearly so adaxially,
raised abaxially. Inflorescence an axillary, bracte- 6. Heisteria Jacq. Fig. 47
ate fascicle, sessile or short-stalked, consisting of
to 15 flowers. Flowers bisexual, 4- or 5-merous, Heisteria Jacq., Enum. Plant. Carib. 4 (1760), nom.
pedicel 5–8 mm long, strongly elongating in fruit, gen. cons. # 2147; Sleumer, Fl. Neotrop. 38: 42–82
the bud globose; calyx ca. cupulate, shallowly (1984), neotrop. spp.
lobed; petals distinct, apex acute, base obtuse,
glabrous abaxially, densely papillate adaxially; Trees or shrubs, rarely scandent. Leaves alternate,
stamens as many as the petals and basally epipe- glabrous, lanceolate, venation pinnate, the
talous, filaments to 1 mm; anthers 4-loculate; laticifers visible against transmitted light.
GENERA OF OLACACAEAE 133
species are characterized by astrosclereids with

various lengths of arms, others have filiform or
columnar sclereids, these three types intergrad-
ing. The most unusual type is the fibrous sclereids
type known from only one species, H. coccinea,
which seems to be nearly equivalent to the ser-
pentine fibers in Notanthera (Loranthaceae). The
genus shows both articulated and non-articulated
laticifers, which is very unusual; vessel members
are said to have scalariform perforation plates.
Heisteria is believed to be autotrophic, an
aspect always difficult to substantiate.
7. Maburea Maas
Maburea Maas, Bot. Jahrb. Syst. 114: 275–291 (1992).
Trees to 25 m high, with grey-black mature and

yellow-brown juvenile bark, young growth with
dense, appressed, whitish hairs. Leaves alternate,
Fig. 47 Olacaceae. A–H Heisteria parvifolia. A Fruiting distichous, petiolate, blade lanceolate to ovate,
branchlet. B Flower. C Stamens, dorsal (left) and ventral
view. D Pistil longitudinally sectioned. E Young fruit with apex shortly acuminate, with 3 or 5 acrodromous
calyx. F, G Mature fruit longitudinally and transversely veins arising from the base, glabrous above,
sectioned. H Embryo. I, J Heisteria zimmereri. I Flowering sparsely hairy below, the 3 largest veins nearly
twig. J Fruit calyx. (Engler 1915) reaching the apex, the main veins connected by
ladder-like cross-veins. Inflorescence a few-flow-
ered cluster, axillary to expanded or aborted
Inflorescences crowded, few- to 20-flowered leaves, or in short spike-like groups. Flowers
clusters in the axils of leaves. Flowers sessile or bisexual, pentamerous, calyx cupulate, the lobes
pedicellate; calyx cupulate, small at anthesis, 5- or deltate; corolla 2 mm long, petals deltate, connate
6-lobed, much accrescent in fruit, becoming a 5- or below, the adaxial side densely covered with erect
6-lobed, often brightly colored cup; petals 5(6), hairs; stamens 10, basally connate with petal tube,
distinct, somewhat hairy or glabrous adaxially, 5 opposite and 5 alternating with the petals, the
caducous; stamens 10(12), rarely 5 or 6, epipeta- two series slightly different in length; ovary supe-
lous/episepalous basally, half of them shorter rior, glabrous, strongly thickened and crenulate,
and opposite the petals, the others longer and 2/3-locular, placentation axile, 1 or 2 ovules per
alternating, filaments slender or flat; anthers locule; style very short, stigma slightly 3-lobed.
small, globular, basifixed, dehiscing longitudinally; Fruit a globular drupe, 1-seeded, endocarp thin
ovary nearly spherical, superior, ovarian cavity and woody Seed ribbed, densely short-pubescent.
3-loculate to just above the middle, with 1 ovule One sp., Maburea trinervis Maas, Guyana.
pendent in each locule from a free, central
funiculus; style very short, short-conical, stigma 8. Olax L.
small, 3-lobed. Fruit a globose to somewhat ovoid
drupe, fruiting calyx much enlarged and subtend- Olax L., Sp. Pl., ed. 1: 34 (1753).
ing or including it, yellowish to variously colored;
pericarp thin and fleshy, endocarp hard, with a Glabrous, semiparasitic trees or shrubs, rarely
single seed. scandent. Leaves alternate, extremely variable in
About 33 spp., mostly in South America as far shape and size, with pinnate venation. Flowers
south as Bolivia (Santa Cruz), with a few species axillary, solitary or in short racemes or spikes,
in Mesoamerica and three in West Africa. with a small, cupulate calyculus, this enlarging
Heisteria shows a remarkable diversity in its in fruit to enclose it nearly entirely; petals 6(5),
foliar sclerenchyma (Baas and Kool 1983). Some distinct or in coherent pairs; stamens 9–12 or
134 Olacaceae
fewer, most fertile but some sterile and often with

deeply 2-lobed sterile anthers, basally epipetalous;
filaments flat, sometimes transversely corrugated;
ovary superior, unilocular or basally 3-lobed, with
3 ovules pendent from the free funiculus. Fruit an
elongated, pyriform to spherical drupe, with a
single seed, completely encased by the enlarged
calyculus. n ¼ 12, 24 (O. nana, O. hypoleuca,
apparently representing tetraploidy).
About 50 spp., paleotropics from Australia to
Madagascar and Africa. Four sections are recog-
nized in Olax, mostly on the basis of staminal
variation: sect. Pentandrae Engler (5–6 stamens
and 3 staminodia), sect. Hemiandrae Engler
(6 stamens and 6 staminodia), sect. Triandrae
Engler (3 stamens and 5 staminodia), and sect.
Estaminodiales Engler (6 stamens, staminodia
lacking).
9. Ptychopetalum Benth.
Ptychopetalum Benth., Hook. J. Bot. 2: 376 (1843).

Fig. 48 Olacaceae. Scorodocarpus borneensis. A Flower-
ing twig. B Flower bud. C Anthetic flower. D Same, petals
Trees or shrubs with alternate, glabrous, some- save one removed. E Drupe. (Sleumer 1984a, drawn by J.
what coriaceous leaves. Inflorescences axillary, van Os)
few-flowered racemes. Flowers bisexual, disty-
lous, with a small, cupulate, weakly 4-toothed petals 5, distinct, bearded adaxially with simple
calyculus, this not enlarging in fruit; petals 4–6, hairs; stamens 10, one fused with each petal mar-
pubescent adaxially; stamens twice as many as gin, the distal filaments being distinct; anthers
the petals, opposite and alternate, the opposite linear; ovary 3–4-chambered, inferior or semi-
ones shorter, some abortive; filaments almost inferior, containing long ovules pendent from
distinct or epipetalous, anthers small, oblong, the nearly free funiculus; style conical, stigma
basifixed; ovary distinct, superior, the single cav- with 3–4 small, acute lobes. Fruit a drupe; exo-
ity nearly filled with a large placenta apically carp thin, endocarp brittle, seed one per fruit.
bearing two or three small, pendent ovules; style One sp., Scorodocarpus borneensis (Baill.)
as long as the ovary, stigma 3-lobed. Fruit a one- Beccari, Malaysia, Sumatra, and Borneo.
seeded drupe, pericarp thin, endosperm copious,
hard, containing fatty substances. 11. Strombosia Blume Fig. 49
Two spp. in tropical South America, and two
in tropical W and C Africa. Strombosia Blume, Bijdr.: 1154 (1826).
10. Scorodocarpus Beccari Fig. 48 Trees, claimed to be autotrophic (Ping 1997),

with glabrous, shiny, coriaceous, entire leaves.
Scorodocarpus Beccari, Nuovo Giorn. Bot. Ital. 9: Flowers small, in short-pedunculate, axillary
274, t. 11 (1877). umbels; calyx small, dish-like, with 5 broad
lobes, distinct or basally united with the ovary,
Tall trees, claimed to be autotrophic (Ping 1997), in fruit enlarged and united with the fruit; petals
with reddish, hard wood. Leaves ovate, coria- 5, distinct, stamens 5, opposite petals and united
ceous. Flowers large, bisexual, in short panicles; with them; anthers ovoid, dorsifixed; ovary infe-
calyx small, with 5 short teeth, not accrescent; rior or semi-inferior, surrounded by a 3–5-lobed
References 135
stamens 4, distinct, opposite the petals, filaments

short, anthers nearly as long as petals, sur-
mounted by a prominent, acute terminal connec-
tive; ovary conical, sunken into the inflorescence
axis, (semi-)inferior, 4-chambered, each locule
with one ovule pendent from the top; stigma
4-lobed. Fruit an (ob)ovoid drupe, with
fleshy sarcocarp and thick endocarp, with a single
seed.
Two spp., tropical West Africa.
13. Tetrastylidium Engler
Tetrastylidium Engler in Mart., Fl. Brasil. 12(2): 33,

t. 7f (1872).
Trees, not known to be parasitic, with thin, long,

lanceolate leaves with acute apex. Flowers short-
pedicelled, in axils of leaves; calyx cupulate,
4-dentate, accrescent in fruit; petals 4, thick,
densely hairy adaxially; stamens 4, basally united
with the petals and opposite them, linear, with
small terminal connectival horn, the pollen sacs
often transversely chambered; ovary elongate,
superior, clasped by a disk-like structure,
Fig. 49 Olacaceae. A–C Strombosia ceylanica. A Flower-
ing branch. B Flower. C Fruit. D, E S. javanica. D Inflores- 4-chambered, with 4 linear pendent ovules from
cence. E Fruit. (Sleumer 1984a, drawn by C. van Os) a central funiculus; stigma nearly sessile. Fruit
drupe-like, encased by the accrescent calyx
except at the very top.
disk, 3-loculed almost to the top, each of the
Two spp., Amazonian Peru and SE Brazil.
locules with one pendent ovule; style short,
stigma weakly 3-lobed. Fruit a drupe with hard
endocarp. n ¼ 20 (40, possibly from endopoly- References
ploidy).
About 16 spp., nine in tropical Africa and Agarwal, S. 1963. Morphological and embryological stud-
seven in tropical Asia. ies in the family Olacaceae I. Olax L. Phytomorphol-
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Baas, P., Kool, R. 1983. Comparative leaf anatomy of
12. Strombosiopsis Engler Heisteria (Olacaceae). Blumea 28: 367–388.
Baas, P., Van Oosterhoud, E., Scholtes, C.J.L. 1982.
Strombosiopsis Engler in Engler & Prantl, Die Nat. Leaf anatomy and classification of the Olacaceae,
Octoknema, and Erythropalum. Allertonia 3:
Pflanzenfam. III, Nachtr. 1: 148 (1897). 155–210.
Barber, C.A. 1907. Studies in root-parasitism. 3. The haus-
Trees or shrubs, not known to be parasitic, with torium of Olax scandens. Mem. Dept. Agric. India,
short internodes. Leaves distichous, petiolate, Bot. Ser. 2(4): 1–47.
Bentham, G., Hooker, J.D. 1862–1883. Genera Plantarum.
coriaceous, apex acute, secondary venation strik- London: Reeve.
ingly scalariform. Inflorescence axillary, short Bonneville, R., Lobreau, D., Riollet, G. 1982. Pollen fossile
and crowded spikes. Flowers each subtended by de Ximenia (Olacaeae) dans le Pléistocène Inférieur
a bract and 2 prophylls, sessile or nearly so in a d’Oldouvai en Tanzanie: implications paléoécologi-
ques. J. Biogeogr. 9: 469–486.
cavity; calyx small, cupulate, 4-toothed; petals 4, Engler, A. 1915. Die Pflanzenwelt Afrikas. III, 1. Leipzig:
distinct, lanceolate, glabrous on both sides; W. Engelmann.
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Feuer, S.M. 1977. Pollen morphology and evolution in the B.J.H. 1992. The identity of “Unknown Z”: Maburea
Santalales, sens. str., a parasitic order of flowering Maas, a new genus of Olacaceae in Guyana. Bot.
plants. Ph.D. Thesis, University of Massachusetts. Jahrb. Syst. 114: 275–291.
Feuer, S.M. 1978. Aperture evolution in the genus Ptycho- Malécot, V., Nickrent, D.L., Baas, P., Van den Oever, L.,
petalum (Olacaceae). Amer. J. Bot. 65: 759–763. Lobreau-Callen, D. 2004. A morphological cladistic
Fineran, B.A., Ingerfeld, M., Patterson, W.D. 1987. Inclu- analysis of Olacaceae. Syst. Bot. 29: 569–586.
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hemi-parasite Olax phyllanthi [sic] (Olacaceae). Pro- 2010. A revised classification of Santalales. Taxon
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Opiliaceae
Opiliaceae (Benth.) Valeton, Crit. Overz. Olacin.: 136 (1886), nom. cons.;
Hiepko, Flora Neotropica 82: 1–53 (2000);
Hiepko, Species Plantarum: Flora of the World 12: 1–71 (2008), rev.
Small or larger trees, more rarely scandent shrubs, wood, in Cansjera even ensheathing the vessels.
8 of the 10 genera being proven root parasites. Wood parenchyma is apotracheal throughout.
Leaves alternate, petiolate, blades often coriaceous Unusually, cystoliths are also found in the wood,
and, when dry, showing fine tubercles of meso- even though this feature is also variable. In the
phyll cystoliths; venation pinnate. Inflorescences leaves, cystoliths are usually abundant, their crys-
usually axillary, sometimes cauliflorous, panicle- talline contents showing diverse shapes. In other
like, racemose, spike-like or umbellate. Flowers leaf cells, crystals may or may not occur, being
small, actinomorphic, mostly pedicellate, mostly absent in Cansjera and minute in Lepioneurus.
bisexual, or plants dioecious; calyculus absent or All genera have at most a very weakly formed
at most weakly differentiated, not enlarging in calyculus, amounting to little more than a constric-
fruit; petals (3)4, or 5, distinct or rarely gamope- tion directly below the petals that is very slightly
talous (lacking in pistillate Agonandra and Gjel- lobed between them. In no case does it enlarge in
lerupia flowers); stamens as many as petals and fruit, as seen in some other families. Hiepko (1984)
opposite them, distinct or connate with the base of does not regard it as a reduced calyx, referring to it
the petals; anthers longitudinally dehiscent; cen- as a slightly cupuliform torus. The glandular, intras-
tral, intrastaminal disk distinct and entire and taminal disk is diagnostic even though variable.
with undulating margin, or with prominent, erect Its lobes are not vasculated, and Hiepko (1984)
lobes alternating with the stamens, evascular; consequently regards them as outgrowths of the
ovary conical to barrel-shaped, superior, unilocu- receptacle rather than staminodes. Also, the single
lar, with a single pendent, unitegmic ovule ovule in a clearly unilocular ovary sets Opiliaceae
attached to the tip of a short funiculus; style apart from other members of the Santalales.
short or lacking. Fruit 1-seeded, with thin, fleshy
sarcocarp and mostly crusty endocarp; endo- CLASSIFICATION. Notwithstanding claims based on
sperm abundant, oily, embryo with 2–4 linear, molecular studies (Nickrent et al. 2010), Antho-
usually 3, closely appressed cotyledons. bolus is here excluded from Opiliaceae and again
Ten genera (4 of them monotypic, and placed in Santalaceae. Contrary to what is stated
another 4 with 3 or 4 spp.) and at least 37 spp., in the above paper, its floral morphology is
mostly paleotropical, Agonandra being the only completely at variance with that of Opiliaceae,
neotropical representative. including the conical, undifferentiated mamelon
lacking differentiated ovules (Stauffer 1959), and
MORPHOLOGY. Koek-Noorman and van Rijckevorsel its affinity with the Santalaceous Exocarpos is
(1983) have provided detailed analyses of the wood undeniable. Otherwise, the family is clearly cir-
and leaf anatomy of 9 genera of Opiliaceae, finding cumscribed morphologically, and on the basis of
a great deal of consistency in the family. Vessels are molecular studies the family is “the most strongly
mostly solitary and diffuse, tracheids are variably supported, monophyletic group in Santalales”,
present, and thick-walled fibers general in the regarded as advanced within the order.
138 Opiliaceae
The accumulating information on the struc- 7. Flowers in short racemes or panicles; petals 4
ture of inflorescences, flowers, ovules, and 9. Rhopalopilia
pollen has led to the recognition of four non- – Flowers in umbels or subumbels; petals 5
ranked groups in the family. The first of these, 8. Pentarhopalopilia
consisting of Gjellerupia, Lepionurus, Opilia, 8. Stigma broad, cushion-like; inflorescence a
Pentarhopalopilia, Rhopalopila, and Urobotrya, branched subumbel; India to Malesia, the Phi-
has racemose inflorescences and pollen grains lippines, and Taiwan 3. Champereia
with a reticulate exine. Secondly, Agonandra – Stigma moderate, not cushion-like; inflores-
also has a racemose inflorescence but has pollen cence otherwise, or flowers single; mostly Afri-
with an echinulate exine. Thirdly, Cansjera has can, some species SE Asia and N Australia 9
spike-like inflorescences and pollen grains with 9. Inflorescence panicle-like, with large, late-
a smooth exine. Finally, Champereia and deciduous bracts; disk lobes separate, erect
Melientha are characterized by panicles and pol- 7. Opilia
len grains with reticulate exine and crested – Inflorescence with small flower clusters, or flow-
muri. ers single; bracts small, early deciduous; glandu-
lar disk undivided 10. Urobotrya
ECONOMIC IMPORTANCE. Except for the local use of
wood of Agonandra, there appear to be no
recorded uses for Opiliaceae. GENERA OF OPILIACEAE
1. Agonandra Miers Fig. 50

KEY TO THE GENERA OF OPILIACEAE
Agonandra Miers, Ann. & Magaz. Nat. Hist. II, 8:
1. Plants dioecious; pistillate flower lacking petals 172 (1851); Hiepko, Flora of the Guianas Newsletter
2 8: 13 (1991), rev.
– Flowers bisexual (rarely polygamous), always
with petals 3
Trees with rather small, ovate to elliptical, thin
2. Disk weakly lobed; ovary conical; New Guinea
leaves. Inflorescence axillary, racemose. Dioe-
4. Gjellerupia
cious. Flowers paired; calyculus-like rim very
– Disk distinctly lobed, the lobes of staminate
small, weakly 4-lobed; staminate flower with 4(5)
flowers with dentate tips; ovary barrel-shaped;
lanceolate, fairly thick petals recurved at anthesis;
tropical America 1. Agonandra
stamens 4, distinct, opposite the petals, with long,
3. Glandular disk lobes triangular, with serrate
slender filaments, anthers globular, more or less
margins 2. Cansjera
basifixed; glandular disk with 4 erect, fleshy,
– Glandular disk simple or with lobes that are not
toothed, basally connate or distinct lobes alternat-
triangular and do not have serrate margins 4
ing with stamens; aborted style minute. Pistillate
4. Petals basally united in urceolate fashion
flower lacking petals and stamens, disk lobes
5. Lepionurus
small but distinct; basal parts of disk lobes mutu-
– Petals distinct or essentially so 5
ally fused in both sexes; ovary barrel-shaped, uni-
5. Ovary globular; flowers bisexual or polygamous;
locular, stigma sessile, weakly 4-lobed, ovule one,
disk lobes of bisexual flowers globular and with
erect. Fruit a spherical, one-seeded drupe with
tubercular surface, those of staminate flowers
fleshy pericarp. Seedling cryptocotylar. n ¼ 10.
flat and more or less spatulate 6. Melientha
Ten spp., Mexico to Paraguay and Argentina.
– Ovary ovoid or at least not globular; flowers
bisexual throughout; disk lobes smooth, not
2. Cansjera Juss.
spatulate or globular, or disk undivided 6
6. Floral pedicels inserted in swollen inflorescence
Cansjera Juss., Gen. 448 (1789), nom. gen. cons. #
axis; petals apically incurved; filaments only
2124; Hiepko, Willdenowia 9: 43–50 (1979).
slightly longer than anthers 7
– Inflorescence axis not swollen at pedicel attach-
ment; petals recurved; filaments at least 2x as Scandent shrubs sometimes with thorns, leaves
long as anthers 8 short-petiolate, alternate. Flowers small, in
GENERA OF OPILIACEAE 139
3. Champereia Griffith
Champereia Griffith, Calc. J. Nat. Hist. 4: 237 (1843);

Hiepko, Willdenowia 9: 14–22 (1979).
Shrubs, sometimes tree-like, with somewhat cori-

aceous, alternate, short-petioled leaves. Inflores-
cence an axillary, branched subumbel; bracts very
small or lacking. Flowers bisexual; calyculus lack-
ing; petals 5, elongated, distinct; stamens 5, oppo-
site the petals, filaments slender, anthers ovoid or
elongate; glandular disk with 5 short lobes, these
not globular or spatulate; ovary ovoid, stigma
broad, cushion-shaped, ovarian cavity single,
containing a single ovule pendent from a central
placenta. Fruit a drupe, embryo with narrow, long
cotyledons.
One sp., C. manillana (Blume) Merr., SE Asia
and Malesia.
4. Gjellerupia Lauterb.
Gjellerupia Lauterb., Nova Guinea 8: 817, t. 149

(1912); Hiepko, Willdenowia 9: 36–38 (1979).
Small trees with alternate leaves. Inflorescence a

Fig. 50 Opiliaceae. Agonandra silvatica. A Branch with short, axillary raceme. Dioecious. Staminate
staminate flowers. B Young staminate inflorescence. flower: calyculus-like rim weakly developed,
C Prophyll of a flower from B. D Adaxial view of a bract. inconspicuously 4-lobed; petals 4, lanceolate;
E Staminate flower. F Three pistillate flowers after anthe- stamens 4, opposite, with long filaments bearing
sis, only one tepal left. G Tepal of pistillate flower.
H Drupe. I Same, lengthwise sectioned. (Hiepko 1993, more or less cordate, exerted anthers; ovary rudi-
drawn by C. Hillmann-Huber) mentary. Pistillate flower: calyculus inconspicu-
ous; petals or stamens lacking; glandular disk
cushion-like, weakly 4-lobed; ovary conical,
short, dense to few-flowered spikes, individual
stigma sessile, locule one, with one ovule.
flowers sometimes with a single bract. Flowers
One sp., G. papuana Lauterb., W New Guinea.
bisexual, calyculus-like rim very weakly devel-
oped, petals 4, united into an urceolate corolla,
5. Lepionurus Blume
basally connate with the long, slender filaments of
the 4 basi-/dorsifixed, opposite stamens; glandu-
Lepionurus Blume, Bijdr. 1148 (1826); Hiepko, Will-
lar disk with 4 large, erect, ovate to triangular
denowia 9: 38–43 (1979).
lobes with serrate margins alternating with the
stamens; ovary conical, stigma with 4 short
lobes, the single ovarian cavity with a central, Shrubs with alternate phyllotaxy, leaves short-
erect funiculus bearing one pendent, anatropous petiolate, elongate. Inflorescence to 3 short pani-
ovule at the tip. Fruit a drupe with thin pericarp cles in axils of bracts; bracts large, enclosing the
and crusty pericarp; embryo small, elongated, young flowers so that the inflorescence looks like
cotyledons 3, strap-shaped. n ¼ 20. a peg, later deciduous. Flowers bisexual, very
Three spp., India, Sri Lanka, S China, New small, calyx small, united with the cup-shaped
Guinea, and N Australia. floral axis, somewhat 4- or 5-lobed; petals 4 or
140 Opiliaceae
5, united with each other and also with the some-

what fleshy glandular disk to form an urceolate
tube; stamens 4 or 5, opposite petals and united
with their bases, filaments short and flat; anthers
ovoid, basifixed or nearly so; ovary conical to
ovoid, style short, stigma weakly 4-lobed, ovule
one, pendent from a central funiculus. Fruit an
ovoid drupe, endocarp crusty, embryo very small,
with 3 cotyledons. n ¼ 10.
One sp., L. sylvestris Blume, from Nepal and
Assam to western Malesia.
6. Melientha Pierre
Melientha Pierre, Bull. Mens. Soc. Linn. Paris 1: 762

(1888); Hiepko, Willdenowia 9: 23–28 (1979).
Trees with alternate, long-lanceolate, short-petio-

late leaves. Flowers small, axillary, fragrant, single
or in small, crowded groups, bisexual or polyga-
mous; calyculus-like rim very small; petals 4 or 5,
ovate, distinct; stamens 4 or 5, opposite the
petals, filaments very short, anthers elliptical,
basifixed; glandular disk represented by 4 or 5
distinct, fleshy lobes that alternate with the petals
and have a tubercular surface; ovary globular,
superior; style absent, stigma broad, sessile, 4-
lobed, with single ovarian cavity containing one
Fig. 51 Opiliaceae. Opilia amentacea. A Three flowers in
ovule at the tip of a short, basal funiculus. Fruit the axil of a fallen bract, one stamen in the open central
an ovoid drupe with single, spherical embryo. flower cut off. B Peltate bract, adaxial view. C Infructes-
One sp., M. suavia Pierre, SE Asia, Borneo, cence with two drupes. D Drupe cut in half, seed removed.
the Philippines. E Seed, longitudinal section. F Twig with young inflores-
cence. (Hiepko 1993; drawn by C. Hillmann-Huber)
7. Opilia Roxb. Fig. 51
single, with one ovule pendent from the central
Opilia Roxb., Pl. Corom. 2: 31, t. 158 (1802); Hiepko, funiculus. Fruit a drupe with thin exocarp and
Willdenowia 12: 161–182 (1982), rev. crusty endocarp; embryo linear. n ¼ 10.
Two spp., often xerophytic, one in tropical
Scandent shrubs, glabrous or somewhat felty. Africa, the other also in tropical Asia, Malesia,
Leaves alternate, coriaceous, petiolate, lanceoate. Solomon Islands, and N Australia.
Inflorescences short panicles with clusters of Opilia was divided into two subgenera by
flowers or single flowers; bracts fairly large, Engler (1909), subgen. (Eu)Opilia and subgen.
short-obovate, late caducous. Flowers bisexual, Urobotrya (Stapf) Engler, the latter strictly Afri-
calyculus-like rim small; petals 4 or 5, distinct; can, the former also in tropical Asia and Austra-
stamens 4 or 5; filaments slender, basifixed or lia. Urobotrya is here presented as a separate
nearly so; glandular disk fleshy, extending into 4 genus (see below). Opilia in the present sense
or 5 large, erect, blunt, glandular lobes that alter- differs from Urobotrya in often having panicle-
nate with the petals; ovary superior, conical or like inflorescences, large inflorescence bracts that
nearly so; style short, stigma blunt; ovarian cavity drop late, and separate, erect disk lobes.
References 141
8. Pentarhopalopilia (Engler) Hiepko 10. Urobotrya Stapf
Pentarhopalopilia (Engler) Hiepko, Bot. Jahrb. Syst. Urobotrya Stapf, J. Linn. Soc. 37: 89 (1904); Hiepko,
108: 280 (1987), rev. ibid. pp. 280–288. Willdenowia 9: 29–36 (1979) (Asian spp.) and in Bot.
Rhopalopila sect. Pentarhopalopilia Engler (1909). Jahrb. 107: 137–152 (1985) (Afric. spp.).
Opilia Roxb. subgen. Urobotrya (Stapf) Engler
See Rhopalopia for vegetative details. Inflores- (1909).
cence an umbel or subumbel. Flower as in Rho-
palopilia, but petals 5, short, oblanceolate, with Plants of the same habit as Opilia, differing in
incurved apex, and with more massive glandular long inflorescences bearing small clusters or sin-
lobes. gle flowers, small, early caducous bracts, and
Four spp., Africa and Madagascar. undivided glandular disk.
Seven spp. in two sections, two spp., W and C
9. Rhopalopilia Pierre Africa, and five spp. from tropical Asia (Thailand
to Flores).
Rhopalopilia Pierre, Bull. Mens. Soc. Linn. Paris 2:
1263 (1896); Hiepko, Bot. Jahrb. 108: 271–291 Excluded: The genus Aveledoa Pittier, listed ten-
(1987). tatively in Sleumer (1935), is presently placed in
Icacinaceae as Metteniusa.
Scandent shrubs with alternate, short-petioled
leaves, venation pinnate. Inflorescence a raceme
or panicle with small flower clusters, the florifer- References
ous axis swollen. Flowers bisexual; calyculus-like
rim small, weakly 4-lobed; petals 4, apically Engler A, 1909. Opiliaceae africanae. Bot. Jahrb. Syst. 43:
175–177.
incurved at anthesis; stamens as many as the Hiepko, P. 1984. Opiliaceae. In: George, A.S. (ed.) Flora of
petals and opposite them, filaments at least as Australia. 22: 26–29.
long as the basifixed, short and broad anthers Hiepko, P. 1987. A revision of Opiliaceae,
with longitudinal dehiscence; glandular disk IV. Rhopalopilia Pierre and Pentarhopalopilia (Eng-
ler) Hiepko gen. nov. Bot. Jahrb. Syst. 108: 280–288.
united and with undulate margin, or with dis- Hiepko, P. 1993. Opiliaceae. In: Fl. Guianas, ser. A, 14.
tinct, erect, blunt lobes alternating with the Koek-Noorman, J., van Rijckevorsel, P. 1983. Wood
stamens; ovary small, broadly conical, unilocular, and leaf anatomy of Opiliaceae. Willdenowia 13:
147–174.
with one pendent ovule from a central funiculus. Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
Fruit a one-seeded, ellipsoid drupe. 2010. A revised classification of Santalales. Taxon
Three spp., tropical Africa. Rhopalopilia had 59: 538–558.
been divided into two sections, sect. (Eu)Rhopa- Sleumer, H. 1935. Opiliaceae. In: Engler, A., Prantl, K., Die
nat. Pflanzenfam., 2nd edn, 16b: 33–41.
lopilia and sect. Pentarhopalopilia (Engler 1909), Stauffer, H.U. 1959. Revisio Anthobolearum. Santalales-
but Hiepko (1987) raised the latter to generic Studien IV. Mitt. Bot. Mus. Univ. Z€ urich 213: 1–260,
status (see above). Pl. 1–24.
Santalaceae
Santalaceae R. Brown (1810).
Thesiaceae Vest (1818).
Amphorogynaceae (Stauffer ex Stearn) Nickrent & Der (2010).
Cervantesiaceae Nickrent & Der (2010).
Comandraceae Nickrent & Der (2010).
Nanodeaceae Nickrent & Der (2010).
Trees, shrubs or herbs, some stoloniferous or ferentiated basal mamelon containing the embryo
with shoots arising from roots, all assumed or sacs. Fruit a drupe, usually with fleshy outer tis-
known to be semiparasitic; stems sometimes sues and hard inner shell, containing a single seed
(Exocarpos) phyllocladic. Leaves alternate, rarely embedded in copious, oily endosperm; germina-
paired, expanded and petiolate or scale-like, or tion mostly epigaeous, rarely (Comandra) hypo-
both, estipulate, mostly glabrous and with pin- gaeous and cryptocotylar (Kuijt 1978).
nate venation. Inflorescences various, or inflores- Thirty-six genera with several hundred spp.,
cences lacking; in Phacellaria, many flowers throughout the temperate and tropical regions of
emerging mostly from just above the internodes, the World; the genus Thesium by far the largest
apparently endogenously (Danser 1939) and with probably more than 300 spp., especially in
flanked by minute bracteoles. Flowers actinomor- arid regions of southern Africa; the family being
phic, usually subtended by a primary bract and absent, except for a single species of Acanthosyris
sometimes, as in some Thesium species and in in Costa Rica, from Mesoamerica and the Carib-
Thesidium, also by two prophylls; bract and pro- bean.
phylls in Quinchamalium connate to envelop the
entire ovary in a sclerenchymatous cover. Pri- VEGETATIVE ANATOMY AND MORPHOLOGY. A curious
mary bract often connate with the floral pedicel, structural feature in the stoloniferous genera
as in Thesium. Flowers mostly bisexual; calyculus Arjona and Comandra is the fact that roots devel-
absent, although a constricted rim may be present oped from the rhizome always take their origin
directly below the petals; petals (3) 4 or 5, valvate, directly above axillary buds (Kuijt 1969). A further
distinct or basally coherent to connate; stamens peculiarity is that the scale-bearing tips of the rhi-
as many as the petals and opposite them, epipe- zomes are recurved, the apical meristems in effect
talous, placed at various heights on the petals, facing backwards. Whether other stoloniferous
and usually with a characteristic tuft of hairs genera like Geocaulon, Nanaodea, Nestronia, and
behind the anthers; filaments often short or lack- Quinchamalium share such features is not known.
ing; a slight basal disk, lobed between petals, Some species of Thesium are also rhizomatous.
sometimes present; anthers short or long, 4-loc-
uled, longitudinally dehiscing; in Choretrum LEAF AND WOOD ANATOMY. The leaves of Santala-
anthers sessile, with 4 globular locules separately ceae have a more or less collenchymatous subder-
dehiscing. Pollen “nearly spherical to ellipsoid, mal layer. Usually, there is a standard division
smooth or finely reticulate”. Ovary inferior of the mesophyll into spongy and palisade
(more or less superior in Anthobolus and Exocar- parenchyma, but some species have anatomically
pos), short or elongate, with one locule, from the isolateral leaves, like Arjona, Jodina, and Lepto-
center of which arises a basal, frequently twisted meria. There are various forms of crystals and
funiculus suspending 3 pendent, ategmic ovules; some sclereids. Vein endings are supplied with
Anthobolus and Exocarpos with a central, undif- small clusters of storage tracheids.
144 Santalaceae
The xylem consists mostly of numerous fiber xylem, most of the interface consisting of paren-
tracheids with bordered pits, with a scattering of chyma. However, in Comandra it is known that
small vessel members characterized by simple endophytic filaments can actively invade the host
perforation plates. The wood of Okoubaka is xylem members. Its endophyte may undergo con-
remarkable in having sparse, wide vessel ele- siderable fragmentation; entry of uniseriate fila-
ments with simple perforations and scattered, ments or single cells through the host’s bordered
vertical, apotracheal wood parenchyma (Nor- pits has been documented, as well as longitudinal
mand 1944). growth of an initially uniseriate filament within a
host tracheary element (Toth and Kuijt 1977). In
PARASITISM. Parasitism has been demonstrated in Exocarpos bidwillii, long and slender, digitate
the great majority of Santalaceae (Kuijt 1969; Der processes form in the endophyte, growing paral-
and Nickrent 2008; Table 4), and is assumed to be lel to the host organ, the innermost portion being
a general feature. The plants may be parasitic on a keel-like ridge that becomes embedded in host
either roots or branches of the host, depending xylem. Individual files of vessel elements with
upon the taxon under discussion. Der and Nickr- simple perforations are present in older portions
ent (2008) have introduced the term amphiphagy (Fineran 1963). In the hyperparasitic genus Pha-
for “species variably root and/or stem parasitic”, cellaria, no study of the endophyte exists, but the
but they appear not to have realized the inherent scattered distribution of shoots emerging from
problems with this concept. Parasitism on stems the endophyte (see Kuijt 1969, his Fig. 3-7a)
in Santalales requires the evolution of specialized surely indicates a very diffuse endophyte.
adhesive tissues that allow seeds to remain
attached to the host during germination, as in INFLORESCENCE STRUCTURE. Inflorescences tend to be
branch-parasitic mistletoes, including those here simple or sparsely branched as in Santalum and
retained in Santalaceae (Kuijt 1990). The great most herbaceous taxa; in form they may be spi-
majority (perhaps all) of these plants have also cate, racemose, or corymb-like. In Phacellaria, we
evolved primary haustoria that frequently have cannot speak of inflorescences unless the entire
evolved further structural or physiological mod- shoot is meant.
ifications of the cell layer that first establishes
contact with the host. The extreme of such mod- FLORAL STRUCTURE AND EMBRYOLOGY. Santalaceous
ifications are seen in Passovia (Loranthaceae; flowers lack a calyx, although a slight constriction
Dobbins and Kuijt 1974). However, such “adhe- below the petals may occur that may be even
sive” modifications are useless in terms of terres- slightly lobed where the 3–5 petals meet. The
trial or hypogeous germination. No known root- petals are mostly distinct but sometimes partly
parasitic Santalales seem to have evolved primary connate below. The ovary is inferior except for
haustoria; equally significantly, no root-parasitic the semi-inferior to nearly superior condition in
members of the order (including the loranthac- Anthobolus and Exocarpos. Nearly all Santalaceae
eous genera Atkinsonia, Gaiadendron, and Nuyt- have bisexual flowers, Geocaulon having 3-flow-
sia) have viscin tissues surrounding their seeds. If ered inflorescences where the middle one is
the root parasitism in the relevant cases turns out bisexual and lateral ones functionally male only.
to be attachments to exposed host roots, then the Stamens are epipetalous and occur in the same
question becomes simpler. It is clear that such number as the petals, usually with short, distinct
aspects are in great need of clarification in the filaments, but in other cases anthers are sessile or
Santalaceous genera involved. nearly so. Both uni- and bisexual flowers occur,
The essential features of the initial phase of especially in Anthobolus and Exocarpos, the latter
haustorial development in Santalaceae have been also showing intermediate conditions (Stauffer
outlined in the introduction to Santalales. Since 1959). It is common, but not universal, to find a
no studies exist of the endophyte per se except in distinctive tuft of hairs on the petal directly
Comandra (Toth and Kuijt 1977) and Exocarpos behind the stamen (Quinchamalium lacks such
bidwillii (Fineran 1964), we may assume it to be, hairs). The style in the family is simple, topped by
in most cases, a relatively simple wedge of tissue a nearly undifferentiated stigma. A basal glandu-
with minor vascular connections to the host lar disk may be present adaxially to the petals, in
Santalaceae 145
a few cases being lobed between them, as espe- octopus-like embryo sac, with upward exten-
cially in Acanthosyris. sions, eventually fills the entire ovarian cavity
As in most members of Santalales, the ovary (Ram 1959). Since most genera of the family
of Santalaceae contains a single chamber in the have not been accounted for in this regard,
center of which stands a structure that represents more unusual situations may well await us.
the evolutionary fusion of a number of ovules,
mostly on a contorted stalk or funiculus. In some POLLEN AND POLLINATION. Pollen in Santalaceae is
genera, like Phacellaria and Quinchamalium, the mostly isopolar, but is distinctly heteropolar in
funiculus is absent, and we find a structure not Anthobolus, Arjona, Comandra, Myoschilos,
unlike the ovarian papilla of most mistletoes. The Mida, Osyridicarpus, Quinchamalium and many,
ovules are greatly reduced; in some genera but not all, species of Thesium. The amb is com-
(Comandra, Thesium), an integument may still monly triangular or nearly so, but tetrahedral in
be recognized, but in others (Santalum, Mida) Myoschilos. Arjona is unusual in having a sharply
the distinction between integument and nucellus triangular amb, one face being separated into
is lost, and in several advanced genera even the three separate portions (Feuer 1977). Sculpting
ovule is scarcely definable. in the family is highly variable, ranging from
Much has been made in the past of the taxo- psilate through tuberculate and areolate to spinu-
nomic significance of major types of embryo sac late. Anthobolus and Exocarpos, while in other
development such as the prevalence of the Polyg- respects very similar, have a very distinct mor-
onum type in all Santalales except Viscaceae and phology in that the former is echinate-perforate
a few others. Zaki and Kuijt (1994, 1995), study- and the latter muricate-striate (Lobreau-Callen
ing Viscum minimum, however, have shown that 1982).
different patterns may exist in a single species, Pollination in Santalaceae has not received
rendering the taxonomic status of this feature much attention, but is apparently effected by
debatable. The same is indicated by the fact that small bees, flies, and beetles. In some Thesium
both of the above types of development occur in species, the flower is known to close during
different species of Olax (Olacaceae; Agarwal adverse weather or at night.
1963).
In a number of genera studied, the embryo KARYOLOGY. Known chromosome numbers in the
sac, like that of Loranthaceae, invades adjacent family include 13, 14, and 26, the latter apparently
gynoecial tissues. The case of Quinchamalium is representing tetraploidy.
perhaps an extreme one, in which the antipodal
end of the embryo sac, sealed off by a cross wall, FRUIT, SEED, AND DISPERSAL. The fruit of Santalaceae
forms a branched haustorial organ reaching into is either a nutlet or a drupe, the latter with a
the apex of the ovarian papilla while the pole fleshy, sometimes brightly colored surface tissue
containing the egg apparatus swells up in clavate as in Geocaulon, Nanodia, and Thesidium. In
fashion. The egg apparatus remains in the papilla Jodina, the fleshy exocarp splits into five easily
but, remarkably, the two synergids each produce detached segments, and similar developments
a slender tube that grows into the style for about occur in Cervantesia and Staufferia. In Exocar-
1/3 of its length (Agarwal 1962). As in some other pos, and to a lesser extent in Anthobolus, the
genera (and in at least some Olacaceae), even the adjacent pedicel swells up and becomes brightly
endosperm produces some haustorial structures. colored, giving rise to the local name “cherry with
Perhaps more representative of the family is the stone outside”, and clearly represents an
the embryo sac of Comandra, where a lateral adaptation to animal dispersal, perhaps the
caecum forms just below the egg apparatus and Casuaris. Thesium alpinum is said to be myrme-
grows into the convoluted funiculus for some chocorous, a small, yellow elaiosome being devel-
distance. Eventually, the endosperm consumes oped from the nearby floral pedicel (Ulbrich
other papillar tissues and even some of the 1907). In the several genera of the family that
ovary wall (Ram 1957). Coalescent, multiple are arboreal parasites, fiber-like processes emerge
endosperm as in Loranthaceae has been reported from the fruit wall upon digestion in the animal
in Santalum (Paliwal 1956). In Exocarpos, an gut that function as attachment structures to
146 Santalaceae
potential host branches when voided (Danser infection in such a plant is difficult to determine.
1940, 1955). Since no significant swellings seem to be present,
and since there is no evidence of shoot generation
GERMINATION AND PARASITISM. In terrestrial Santala- from within host tissues, the structure of the haus-
ceae, germination mostly appears to be epigeous, torium almost certainly is a simple, limited one
that of Comandra, Santalum, and Thesium being similar to that elsewhere in the family.
hypogeous; however, seedlings of the great The haustoria of Buckleya are reported to
majority of the genera involved have not been remain alive (and presumably functional) for at
described. In Comandra (Kuijt 1978) and Santa- least 15 years (Kusano 1902).
lum, we find instances of cryptocotylar germina- As far as known (with the above reservation
tion. on Phacellaria), the endophyte of Santalceae is a
The most intriguing members of the family fairly simple wedge of tissue, with connections to
undoubtedly are the branch-parasitic mistletoes host xylem and especially parenchyma. It is only
of tropical Asia and northern Australia, especially in Comadra (Toth and Kuijt 1977) that a degree of
the unique, squamate genus Phacellaria that very endophytic fragmentation has been documented;
much resembles Arceuthobium in Viscaceae. from marginal areas, individual filaments of the
Unfortunately, there are some important gaps in endophyte may even grow into the length of a host
our knowledge about some of these genera, and xylary member, terminating in a single apical cell.
their taxonomic status is by no means clear. Pha-
cellaria, however, is a very distinctive taxon, HOSTS. As in most root parasites, little is known
sharply delimited from the others, and probably about the host ranges in Santalaceae. The excep-
representing a quite separate line of evolution. tion, understandably, is in the genus Phacellaria,
From herbarium material—and by extrapolation which is limited to other mistletoes, mainly Lor-
from Arceuthobium—we may make certain anthaceae and Viscaceae (Danser 1939). The indi-
deductions. Specimens often produce a swelling cations that elsewhere are available point to a lack
on the primary host, always another mistletoe of specificity in host choice, as in Anthobolus and
(Loranthaceae or another santalaceous mistle- Exocarpos (Stauffer 1959). Barber (1906) men-
toe). Shoots are generated from the endophyte, tions more than a hundred hosts species for San-
often over a length of 10 cm (see illustrations in talum album, and Pizzoni (1906) gives a similar
Danser 1939, who writes that stems emerge from report for Osyris alba. Buckleya distichophylla
host lenticels). These two facts signify that the seemed to prefer the roots of Tsuga canadensis
endophyte is a greatly fragmented system, until this was shown to be only a matter of co-
penetrating the host branch in both directions, occurrence (Piehl 1965). The same was true for
in all likelihood through the cortex and phloem, Pyrularia until at least 63 host species of numer-
as in Arceuthobium. It may also be suggested that ous genera and families were documented by
early penetration probably proceeds from a pri- Leopold and Muller (1983). Nestronia also
mary haustorium representing the tip of the radi- scarcely appears to be host specific. As mentioned
cle, as in other advanced parasitic angiosperms. It elsewhere, however, the identification of hosts in
would be interesting to find that, again as in other root parasites is usually a very cumbersome and
highly advanced mistletoes (Arceuthobium, Kuijt labor-intensive enterprise, and generalizations
1960; Viscum minimum, Kuijt 1986; Tristerix may be premature.
aphyllus, Kuijt 1988), all shoots are generated
from the endophyte, the epicotylar portion of DISTRIBUTION. Santalaceae are found throughout
the seedling withering away following host the temperate and tropical world, the genus The-
entry. Careful field observations are needed, but sium with perhaps more than 300 species being
their obvious difficulty lies in the host inaccessi- especially common in arid southern Africa. There
bility in the canopy of trees. is an unexplained large gap in family distribution
The other Asiatic ramal parasites have a very in the Caribbean area, where no species are
different habit from Phacellaria. They tend to form known, and in northern South America and
an irregular mass of partly creeping and intertwin- Mesoamerica where, in the latter area, only
ing growth on host stems. The primary locus of Acanthosyris is known, and that only very rarely.
Santalaceae 147
Even though molecular considerations have monophyletic assemblage. The latter family was
prompted Der and Nickrent (2008) and Nickrent nevertheless retained “as this option results in
et al. (2010) to move Anthobolus to Opiliaceae, I less disruption of the existing system where it
have been unable to devise a family description for [Viscaceae] is well established and frequently
that family that would include the genus. Anthobo- used.” The recognition of the other six families
lus flowers have essentially sessile anthers, while was considered a cladistic consequence of or rather
those of Opiliaceae have distinct, often long, fila- a sacrifice for maintaining Viscaceae as a family.
ments. More important is the fact that no promi- It has, however, proven exceedingly difficult
nent disk or disk lobes exist in Anthobolus, while to establish meaningful taxonomic distinctions
this is a defining feature in Opiliaceae. Nickrent between several of the resultant families, and the
et al. (2010) write of a calyculus in Anthobolus, internal integrity of some of them seems dubious.
but that is an error. Cystoliths are present in the In Nanodeaceae, for example, the claimed calycu-
leaves of Opiliaceae, but not in Anthobolus, an lus in Nanodea and Mida does not exist, and the
essentially leafless shrub. Finally, Anthobolus lacks “tetramerous” flower of the latter, in reality, is
differentiated ovules, instead forming a mamelon- pentamerous (Cheeseman 1914). Nothing is
like structure like that of mistletoes and Exocarpos, known about the embryology of Nanodea, and
while Opiliaceae are characterized by a single, well- this minute plant is scarcely a subshrub, contrary
differentiated, pendent ovule (Stauffer 1959). to what the authors imply (see Fig. 56 below). All
Anthobolus is thus again included in Santalaceae this renders the combination of these two genera
in the present treatment where nearly all modern in one family very questionable. Another prob-
students, especially the monographer Stauffer, have lem is seen in the fact that the genus Anthobolus
located it near Exocarpos. is removed from Santalaceae and placed in Opi-
liaceae. Contrary to the authors’ statement, that
FOSSILS. The only more or less reliable Santalac- genus is not at all morphologically compatible
eous fossils are a Thesium-like flower and two with Opiliacae, and in the present treatment is
staminate flowers of Osyris from amber deposits restored to Santalaceae where both Stauffer’s
in the Baltic Sea area (Pilger 1935). monograph (1959) and P. Hiepko’s personal
judgment placed it. A third example of conflict
HUMAN USES. Sandalwood trade. Santalum album is present in the authors’ inclusion of both Arjona
and several related Santalum species continue to and Quichamalium in Schoepfiaceae. Schoepfia is
have significant commercial value because of the a pantropical shrub to 10 m high, differing in the
dense heartwood and the famous, fragrant essen- inflorescence and other details; especially Arjona
tial oils; more details are provided in the introduc- shows overwhelming correspondences with the
tion to Santalales. On the Juan Fernández Islands, Northern Hemisphere genus Comandra. The lat-
this has led to the extermination of the native ter genus, placed with Geocaulon in a separate
species S. fernandezianum (Mida salicifolia), one family, Comandraceae, is virtually impossible to
of two parasitic plants that have become extinct in separate from other Santalaceae at a family level.
recent history (the New Zealand mistletoe Trilepi- An admittedly difficult decision has here been to
dia adamsii being the other extinct species). retain Eremolepidaceae as a family, as its deriva-
tion from Santalaceae seems well established, but
Other uses. Tubers of some Arjona species are I see it as a uniquely American evolutionary
eaten by aboriginal peoples in southern Chile experiment involving, in at least one case, the
(Skottsberg 1916). independent origin of epicortical roots and, in
all three genera, the independent origin of the
SYSTEMATICS. Since my treatment of Santalaceae dif- primary haustorium and arboreal parasitism. In
fers in significant respects from that of Nickrent summary, I see no alternative but to return to the
et al. (2010), it is necessary to provide a justifica- traditional view of Santalaceae.
tion of my views. In that study, an extreme position Since various novel family placements for
was taken in recognizing six families in what tradi- erstwhile Santalalean genera have been suggested
tionally has been a single one, Santalaceae, s.l. It is mostly by Nickrent et al. (2010), it may be useful
apparent from the consensus phylogeny produced to summarize the different classifications in the
that those six families, plus Viscaceae, represent a following table.
148 Santalaceae
Table 6 Family disposition of genera related to Santalaceae, s.l

Pilger (1935) or others Nickrent et al. (2010) Present treatment
Acanthosyris Santalaceae Cervantesiaceae Santalaceae
Amphorogyne Stauffer and H€ urlimann (1957)
Santalaceae Amphorogynaceae Santalaceae
Anthobolus Santalaceae Opiliaceae Santalaceae
Antidaphne Engler and Krause (1935)
Loranthaceae Santalaceae Eremolepidaceae
Arjona Santalaceae Schoepfiaceae Santalaceae
Buckleya Santalaceae Thesiaceae Santalaceae
Cervantesia Santalaceae Cervantesiaceae Santalaceae
Choretrum Santalaceae Amphorogynaceae Santalaceae
Colpoon Santalaceae Santalaceae Santalaceae
Comandra Santalaceae Comandraceae Santalaceae
Daenikera H€urlimann and Stauffer (1957)
Dendromyza Danser (1940)
Dendrotrophe Miquel (1856)
Dufrenoya Chatin (1860)
Eubrachion Engler and Krause (1935)
Exocarpos Santalaceae Santalaceae Santalaceae
Geocaulon Santalaceae Comandraceae Santalaceae
Jodina Santalaceae Cervantesiaceae Santalaceae
Kunkeliella Stearn (1972)
Santalaceae Thesiaceae Santalaceae
Lepidoceras Engler and Prantl (1935)
Leptomeria Santalaceae Amphorogynaceae Santalaceae
Mida Santalaceae Nanodeaceae Santalaceae
Myoschilos Santalaceae Santalaceae Santalaceae
Nanodea Santalaceae Nanodeaceae Santalaceae
Nestronia Santalaceae Santalaceae Santalaceae
Okoubaka Pellegrin and Normand (1946)
Santalaceae Cervantesiaceae Santalaceae
Omphacomeria Santalaceae Santalaceae Santalaceae
Osyridicarpus Santalaceae Thesiaceae Santalaceae
Osyris Santalaceae Santalaceae Santalaceae
Phacellaria Santalaceae Amphorogynaceae Santalaceae
Pilgerina Rogers et al. (2008)
Pyrularia Santalaceae Cervantesiaceae Santalaceae
Quinchamalium Santalaceae Schoepfiaceae Santalaceae
Rhoiacarpos Santalaceae Santalaceae Santalaceae
Santalum Santalaceae Santalaceae Santalaceae
Scleropyrum Santalaceae Cervantesiaceae Santalaceae
Spirogardnera Stauffer (1968)
Staufferia Rogers et al. (2008)
Thesidium Santalaceae Thesiaceae Santalaceae
Thesium Santalaceae Thesiaceae Santalaceae
KEY TO THE GENERA OF SANTALACEAE 149
KEY TO THE GENERA OF SANTALACEAE 12. Herbaceous plants, excluding those with a woody
base and Daenikera 13
1. Asiatic or Australian plants parasitic on branches, – Woody plants, including those with a woody base and
hyperparasitic on other mistletoes, or scandent on Daenikera 19
tree branches 2 13. South America 16
– Terrestrial plants (rarely attached to, or emerging – Native to North America (Thesium introduced locally
from host stems: Daenikera); Old or New World; not in Montana), Eurasia, or Africa (including Madagascar;
hyperparasitic or scandent 4 one species of Thesium in SE Australia/Tasmania) 14
2. Plants squamate, hyperparasitic, emerging from the 14. Plants glabrous or hairy, including floral parts; fruit
host in clustered fashion; India and Malaysia to S a nutlet with distinctive surface veins; mostly Africa,
China 26. Phacellaria Europe, Madagascar, SE Australia, Tasmania
– - Plants at least partly foliaceous, not hyperparasitic; 36. Thesium
Himalayas to New Guinea, New Caledonia, or N Aus- – Plants and floral parts glabrous; fruit a drupe or
tralia 3 nutlet, its surface smooth; North America (Comandra
3. Plants with non-twining, foliaceous stems, lacking also in the Balkan area) 15
epicortical roots or secondary haustoria 15. Inflorescences terminal, with numerous bisexual
12. Dufrenoya flowers; fruit greenish 9. Comandra
– Plants with twining, squamate stems producing sec- – nflorescences 3-flowered, axillary; lateral flowers
ondary haustoria as well as straight, foliaceous, non- functionally male, central flower bisexual or pistillate;
haustorial stem fruit orange 14. Geocaulon
11a & 11b. Dendrotrophe & Dendromyza 16. Small, creeping herb; flowers in axillary groups of 3;
4. Phyllotaxy mostly paired or whorled 5 petals 4, not formed into tube; the 4 more or less
– Phyllotaxy consistently alternate 11 distinct stamens inserted on base of petals; fruit a red
5. Phyllotaxy whorled; New Caledonia drupe, exocarp fleshy. Extreme southern South
2. Amphorogyne America and Falklands Islands
– Phyllotaxy mostly paired; leaves lanceolate, apex 20. Nanodea
acute; not on New Caledonia (except one species of – Erect plants; petals connate into a short or long floral
Santalum with acute leaves) 7 tube, the stamens attached near its mouth; fruit a
7. Each pistillate flower solitary at the tip of a leafy nutlet 17
shoot, with 4 long foliar bracts alternating with petals; 17. Nutlet surface veined; S Brazil
staminate flowers lacking post-staminal hairs 35. Thesium brasiliensis & T. aphyllum
5. Buckleya – Nutlet surface not veined 18
– Flowers mostly bisexual, or pistillate flowers either in 18. Ovary and dry fruit ensheathed by a 3-toothed scle-
axillary umbels or in panicles; post-staminal hairs renchyma envelope; subterranean tubers lacking
present; flowers lacking foliaceous bracts 8 29. Quinchamalium
8. Rhizomatous shrub, dioecious or flowers bisexual; – Ovary and fruit distinct; rhizome tips swelling tuber-
flowers in axillary umbels 21. Nestronia like 4. Arjona
– Non-rhizomatous shrubs or trees; flowers mostly or 19. New World 20
always bisexual, inflorescence an axillary or terminal – Old World 25
cyme or panicle 9 20. Plants with short shoots, often in axils of spines;
9. Branches complanate; petals 4; fruit a drupe glandular disk with conspicuous, lateral, petal-like
8. Colpoon lobes 1. Acanthosyris
– Branches terete or quadrangular when young; petals 4 – Short shoots absent; glandular disk without petal-like
or 5; fruit a nut 10 lobes 21
10. Stems quadrangular when young; inflorescence a 21. Leaves rhombic in shape, each side and the apex with
small axillary, 1–5-flowered cyme; E South Africa a prominent spine 14. Jodina
30. Rhoiacarpos – Leaves otherwise, lacking lateral or terminal spines 22
– Stems terete when young; inflorescence an axillary or 22. Inflorescence a raceme but not catkin-like; E and SE
terminal panicle, often many-flowered; not known United States 28. Pyrularia
from South Africa 31. Santalum – Inflorescence catkin-like or a short cluster or cyme;
11. Stiffly erect, dark purple, essentially leafless shrublet; South America 23
New Caledonia 10. Daenikera 23. Young growth usually densely pilose, sometimes glab-
– Erect or not, but not dark purple; leaves or leaf scales rescent; exocarp fleshy, splitting into 5 long segments
numerous, evident, rarely caducous; New Caledonia reaching to the base 6. Cervantesia
or elsewhere 12
150 Santalaceae
36. Flowers sessile; inflorescence with stellate pubescence

– Plants glabrous, fruit a drupe or nutlet but exocarp
22. Okoubaka
not splitting at maturity 24
– Flowers pedicellate or, if sessile, inflorescence without
24. Inflorescence catkin-like; flowers sessile; petals dis-
stellate pubescence 37
tinct; fruit a drupe. Argentina and adjacent Chile
37. Twigs angular when young; petals 3 or 4; Mediterra-
19. Myoschilos
nean and Africa to China 25. Osyris
– Inflorescence not catkin-like; flowers pedicellate;
– Twigs not angular when young; petals 4 or 5; Africa,
petals basally connate; fruit a nutlet; southern Brazil
Ceylon, India to New Guinea 38
36. Thesium brasiliensis & T. aphyllum
38. Inflorescence mostly a 3-flowered cyme; Africa
25. Australia, New Zealand, or SW Pacific Islands 26
24. Osyridicarpos
– Eurasia-Africa, including Madagascar and New
– Inflorescence spike-like, racemic, or catkin-like; Cey-
Guinea 32
lon and India to New Guinea
26. Petals conspicuously constricted basally; fruit trun-
32. Scleropyrum
cate apically; New Zealand (North Island); extinct on
39. Drupe strongly 5-grooved 34. Staufferia
Juan Fernández Islands 18. Mida
– Drupe not 5-grooved 27. Pilgerina
– Petals without basal constriction; fruit not apically
40. Flower with 1 bract and 2 bracteoles; drupe grooved;
truncate; Australia (Exocarpos bidwillii in New Zeal-
Canary Islands 16. Kunkeliella
and) 27
27. Ovary superior; receptacle often enlarged and fleshy – Flower lacking bracteoles; fruit smooth; not on
below drupe 28 Canary Islands 41
41. Base of fruit surrounded or clasped by swollen, bright-
– Ovary (semi-) inferior; receptacle not enlarged or
colored pedicel 13. Exocarpos
fleshy below drupe 30
28. Flowers prominently stalked 3. Anthobolus – Base of fruit lacking expanded pedicel 42
42. Leaves leathery, linear to broadly elliptical, to 5 cm
– Flowers sessile or nearly so 29
long; fruit mostly spherical; Mediterranean and mon-
29. Plants dioecious; drupe more or less sessile, 6–7 mm
tane paleotropics 25. Osyris
long; receptacle not enlarged below drupe
23. Omphacomeria – Leaves leathery or thin, not linear, to 15(20) cm long;
fruit mostly pyriform; E USA and parts of SE Asia 43
– Flowers bisexual; receptacle enlarged and fleshy
43. Leaves leathery; Sri Lanka, India, Malacca, Laos, New
below drupe; drupe up to 5 mm long
Guinea 32. Scleropyrum
13. Exocarpos
30. Flowers in terminal, spiral spikes, without bracts – Leaves thin; E and SE USA, and Central to E Hima-
33. Spirogardnera layas 28. Pyrularia
– Flowers in axillary or lateral racemes or clusters, sub-
tended by a bract or bracteoles 31
31. Each flower subtended by 2 or more bracts GENERA OF SANTALACEAE
7. Choretrum
– Each flower subtended by a single bract
1. Acanthosyris (Eichler) Griseb.
17. Leptomeria
32. Shrubs; petals basally connate; fruit a small nutlet with
Acanthosyris (Eichler) Griseb., Goetting. Abhandl. 24:
conspicuous surface venation
151 (1871).
36. Thesium
Osyris sect. Acanthosyris Eichler (1868).
– Trees or shrubs; petals not basally connate; fruit often
a drupe, its surface smooth 33
33. Mediterranean to China, or Africa, including Mada- Trees or shrubs, often with thorns and/or short
gascar 34 shoots subtended by the ovate-elliptical or falcate,
– Neither Mediterranean nor African-Madagascan (but alternate leaves; spines subtending short or long
Canary Islands included) 40 shoots, or spines absent, young organs in part
34. Madagascar 39 pubescent (incl. the abaxial surface of petals) or
– Mainland Africa and tropical Asia 35 glabrescent. Inflorescence a short-pedunculate
35. Each flower with 2 prophylls cyme of 3–5 flowers, axillary to the scale leaves at
35. Thesidium the base of short shoots or spines. Flowers bisexual,
– Flowers lacking prophylls 36 fragrant, mostly 5-merous; post-staminal hairs
GENERA OF SANTALACEAE 151
present; stamens as many as petals; stamen fila- terete to angular. Leaves alternate, linear to lance-
ments short, thick, distinct, perhaps adhering to olate, apetiolate or nearly so, often caducous.
the adjacent petals by its sticky hairs, basally Inflorescences axillary, few-flowered racemes, the
attached to and opposite the petals; glandular disk staminate 3–8-flowered, pistillate mostly 1-flow-
extending into prominent, somewhat fleshy lobes ered. Dioecious. Flowers pedicellate, with 3–5
between the petals; ovary semi-inferior; ovules 3, petals. Staminate flowers: petals oval to deltoid,
pendent from the top of a convoluted funiculus lacking calyculus or articulation below the petals;
but facing upwards. Fruit globular, nut-like, petals stamens as many as the petals, opposite and united
persistent, but exocarp fleshy, greenish to yellowish- basally with the petals; anthers 2-loculed, dorsi- or
orange, edible; endosperm solid, embryo extremely basifixed, dehiscing with a longitudinal slit; post-
small. staminal hairs absent; filaments very short, disk
Five spp., South America, from S Brazil, SE small, vestigial style lacking; pollen tricolporate.
Bolivia and Uruguay to the Rı́o Paraguay estuary. Pistillate flower: petals tongue-shaped, articulate
A new species, A. annonagustata, has been descri- at their base, this resembling a very small calycu-
bed from E Ecuador (Ulloa and Jorgensen 1998) and lus; sterile stamens and disk lacking; ovary supe-
has recently been collected in Costa Rica, suggesting rior, conical-ovoid, stigma sessile, 3–5-lobed;
that it may be present in Panama as well. ovarian cavity simple, placenta conical, ovules
not differentiated. Fruit ca. ellipsoid, the pedicel
2. Amphorogyne Stauffer & H€
urlim. swollen and elongated; exocarp red to orange,
mesocarp fleshy and sticky, endocarp bony, finely
Amphorogyne Stauffer & H€ urlim., Vierteljahrsschr. Nat- grooved. Seed solitary, embryo dicotylous.
urforsch. Gesellsch. Z€
urich 102: 337–349 (1957). Three spp., northern half of Australia.
Molecular data have led Nickrent et al. (2010)
Shrubs or small trees, glabrous, with forked branch- to place Anthobolus in Opiliaceae, but there are
ing; innovations of a single internode terminated by several strong arguments against that view, as
a whorl of (usually) 4 leaves. Leaves leathery, oblan- described above under the family discussion.
ceolate to spatulate, apex rounded, often with small
mucro, base tapering to very short petiole, venation 4. Arjona Cav.
pinnate, the midvein raised abaxially. Inflores-
cences racemose, axillary (or terminal?), lateral Arjona Cav., Icon. 4: 57, t. 383 (1797).
units single, pedicellate flowers or few-flowered,
pedunculate groups. Flowers pedicellate; petals 5 Rhizomatous, herbaceous plants or (more rarely)
(6), deltoid; stamens as many as the petals and subshrubs, some rhizomes swelling into small
basally united with them, with post-staminal hair fusiform (edible) tubers that regenerate the
tufts; filaments short; anthers bilocular, dorsifixed; plant in the following growing season, the rhi-
ovary inferior, indistinguishable from the tapered zome tip recurved. Shoots dimorphic, some
pedicel; style short and stout, stigma truncate, unbranched and sterile, others terminating in an
somewhat 3- or 4-lobed. Fruit a one-seeded, ellip- inflorescence. Leaves alternate, linear to lanceo-
soid drupe; exocarp membranaceous, mesocarp late, stiff, acute. Inflorescence a terminal spike of
fleshy, endocarp hard, embryo dicotylous. crowded, white to purplish red flowers. Flowers
Two spp., endemic to New Caledonia. bisexual, distylous, the 4 or 5 petals basally united
3. Anthobolus R. Br. into a tube that is often hairy outside; stamens
with short filaments attached to mouth of tube;
Anthobolus R. Br., Prodr. Fl. Nov. Holl. (1810); Stauffer, post-staminal hairs present; glandular disk cush-
Mitteil. Bot. Mus. Univ. Z€ urich 213: 1–260, tab. 1–3 ion- or ring-shaped, persistent on the fruit; ovary
(1959), rev. inferior; calyculus not recognizable; style fila-
mentous, exceeding the floral tube; stigma
Xerophytic, glabrous, much branched shrubs, 3-lobed; ovules 3, pendent from a central, stout,
sometimes leafless, semiparasitic; internodes straight funiculus. Fruit a small nutlet. n ¼ 14.
152 Santalaceae
About a dozen spp., N from Tierra del Fuego drupe-like, red or blue, 1-seeded, exocarp fleshy,
at least as far as Peru, Argentina, and southern divided into 5 long segments reaching to the base,
Brazil. endocarp stony, usually with 2 or 3 long slits.
Molecular evidence has led Nickrent et al. Seed spherical, embryo dicotylous.
(2010) to place Arjona (with Quinchamalium) in Three or four spp., Peru and Ecuador.
their Schoepfiaceae (Olacaceae), a suggestion that
is here rejected. 7. Choretrum R. Br.
5. Buckleya Torrey Choretrum R. Br., Prodr. Fl. Nov. Holl. 1: 354 (1810).
Buckleya Torrey, Amer. J. Sc. 45: 170 (1843), nom. cons. # Small shrub often with rod-like branches, much
2109; Carvell & Eshbaugh, Castanea 47: 17–37 (1982), rev. branched, with small, usually long-persistent,
alternate scale-leaves. Flowers small, solitary or
Shrubs; leaves narrowly ovate leaves with short clustered, axillary, each with 2 or more small
petioles and acute apex, phyllotaxy decussate. bracteoles, bisexual, often with small teeth
Dioecious, sterile organs of the opposite sex lack- between the petals; petals 5, thick, erect, the
ing. Male inflorescence a small umbel, staminate acute tip bent inwards, covering the 5 epipetalous
flowers small, without calyculus; petals 4, each stamens; glandular disk weakly 5-lobed; filaments
basally with an epipetalous stamen; post-staminal very short, anthers dorsifixed, with 4 inward-fac-
hairs absent; glandular disk prominent, square. ing locules dehiscencing introrsely and sepa-
Pistillate flowers solitary at the end of leafy shoots, rately; style very short, stigma 5-lobed; ovary
subtended by pairs of scale leaves; the 4 deltoid broadly top-shaped, semi-inferior, united with
petals alternating with 4 elongated green bract-like the obconical pedicel. Fruit globular to ellipsoid,
organs; glandular disk square; style straight, bearing the persistent petals; exocarp thin, coria-
stigma 4-lobed; ovary inferior, much elongated; ceous-fleshy, endocarp stony, thick.
ovules 3 or 4, very small, pendent from the tip of Six spp., Australia.
a central funiculus. Fruit a dry nut, exocarp thin,
endocarp stony, embryo dicotylous. 8. Colpoon P. J. Bergius
Five spp., one in E North America, 4 in E Asia.
Colpoon P.J. Bergius, Descr. Pl. Cap. Bon. Spei 38, t. 1, fig.
6. Cervantesia Ruı́z & Pavón 1 (1767).
Cervantesia Ruı́z & Pavón, Fl. Peruv. Chil. Prodr.: 39, t. 7 Small trees or shrubs with complanate branches.
(1794). Leaves paired (more or less alternate on very
vigorous shoots), coriaceous, elliptical to
Small trees with ovate to elliptical, alternate obovate. Inflorescences small, terminal racemes,
leaves, young growth and abaxial leaves densely naked below and distally with small, nearly capi-
pilose, less so adaxially, or glabrescent. Inflores- tate clusters of to 10 flowers, with caducous, nar-
cences small clusters of flowers, axillary or in row bracts. Flowers bisexual or pistillate with
terminal arrangement. Leaves alternate, the aborted stamens; petals 4, blunt; stamens 4, oppo-
blades ovate to elliptical, sometimes coriaceous. site, short, with sparse post-staminal hairs;
Flowers bisexual; petals 5, with associated post- anthers with 4 locules, longitudinally dehiscent;
staminal hairs; stamens with short filaments, epi- glandular disk weakly 4-lobed; ovary inferior;
petalous; anthers with 4 elongated locules dehisc- style short, stigma with 4 short lobes; ovarian
ing with a combined longitudinal slit; receptacle cavity simple; ovules 4 or 5, pendent from a
somewhat cupular around the ovary, which is stout, central funiculus, facing upwards. Fruit a
initially distinct but gradually becomes nearly drupe with enlarged pedicel, reddish to brown,
inferior; style short, stout, stigma indistinctly 2- obovoid or ellipsoid, bearing the persistent
or 3-lobed; ovarian cavity simple, with contorted petals; exocarp fleshy, endocarp stony; embryo
funiculus and 2 or 3 apically pendent ovules. Fruit dicotylous, cotyledons very short.
One sp., Colpoon compressum P.J. Bergius, This curious species has been said to be
South Africa. amhiphagous (H€ urlimann and Stauffer 1957;
Nickrent et al. 2010). It is puzzling to find it
9. Comandra Nuttall attached to both host roots and host stems
because each location requires a very different
Comandra Nuttall, Gen. N. Amer. Pl. 1: 157 (1818); Piehl, germination and establishment regime. It is con-
Mem. Torrey Bot. Club 22: 1–97 (1965), rev. ceivable that entrance took place subterra-
neously, structures like cortical stand
Perennial, glabrous, rhizomatous plants to 30 cm traversing tissues into the stem and emerging
high; rhizomes stout, their roots with numerous there as shoots. For a discussion of the amphi-
haustoria, the subterminal portions swollen into phagy concept, see the introductory portions of
slender tubers, the rhizome tips curved back- the order.
wards; shoots dimorphic, some vegetative,
unbranched, others with a terminal inflorescence. 11a. Dendrotrophe Miquel
Leaves lanceolate, often glaucous when exposed.
Inflorescence branched, with numerous, bisexual, Dendrotrophe Miquel, Fl. Ind. Bat. 1: 779 (1856).
whitish to pinkish flowers subtended by small,
linear bracts. Flowers bisexual; petals (4) 5, 11b. Dendromyza Danser
stamens as many, united basally with the petals
and backed by a tuft of hairs; glandular lobes Dendromyza Danser, Nova Guinea, N.S., 4: 133 (1940);
alternating with the petals; ovary inferior, obco- Danser, Nova Guinea, N.S., 6: 261–277, tab. 9–24 (1955),
nical; style conical at the base, filamentous above; rev.
ovarian cavity simple, with 2 or 3 ovules pendent Henslowia Blume (1850), p.p.
from contorted central funiculus. Fruit a dry, Cladomyza Danser (1940).
greenish-grey drupe, the petals persistent. n¼13,
26, the latter for C. umbellata subsp. pallida. Small bushes, some at least partly scandent, para-
One sp., C. umbellata Nuttall, N North Amer- sitic on tree branches; leaves alternate. Flowers
ica, the Balkans Peninsula and Romania. very small, in small, axillary clusters or solitary,
rarely bisexual, more commonly plants dioecious
10. Daenikera H€
urlim. & Stauffer or monoecious; petals 5 or 6. Staminate flowers
with flat receptacle; stamens with very short fila-
Daenikera H€ urlim. & Stauffer, Vierteljahrsschrift Natur- ment, epipetalous on petal base, post-staminal
forsch. Gesellsch. Z€
urich 102: 332 (1957). hairs present; anthers small, at the tip of the
filament, dehiscing transversely. Pistillate flower
Small, erect, nearly leafless root parasite, purplish with or without small sterile stamens; ovary infe-
when fresh, glabrous, the lowest internodes much rior; glandular disk concave or convex; stigma
elongated. Inflorescence a small panicle with ter- essentially sessile, with 2–5 lobes; ovarian cavity
minal flower below which are single flowers and simple; ovules 2 or 3, pendent from the tip of a
triads in the axils of alternate bracts. Flowers short, thick placental column. Fruit a small
minute, short-pedicellate, unisexual? Petals 4, drupe, spherical to ovoid; exocarp fleshy, endo-
ovate, erect, purplish; stamens (staminodia?) carp hard. Seed solitary, with prominent longitu-
with one or two locules, anther dorsifixed on dinal furrows; embryo with 2 cotyledons, these
short filament, this united with the base of the often connate.
petals; post-staminal hairs sparse; ovary more or At least 21, poorly known spp., India to S
less inferior, the (glandular?) part above the China, the Philippines, Melanesia and N Austra-
petals depressed-conical, grading into a very lia.
short style; stigma 2(3)-lobed; ovarian cavity sim- The genera Dendromyza and Dendrotrophe at
ple, with 2 ovules attached to a short funiculus. present seem inadequately separated and are pro-
Fruit a globular, small drupe or nut bearing the visionally placed together in the present treat-
persistent petals, single-seeded. ment. The only generic contrasts in Danser’s
One sp., Daenikera corallina H€ urlim. & Stauf- writing seem to lie in the nature of the mesocarp
fer; New Caledonia. fibers and the surface features of the endocarp
154 Santalaceae
(smooth in Dendromyza, more or less tuberculate 12. Dufrenoya Chatin

in Dendrotrophe). It is unfortunate that Danser
was never able to revise Dendrotrophe, his 1940 Dufrenoya Chatin, Compt. Rend. Acad. Paris 51: 657
listing of 10 species being but a preliminary (1860).
effort; his 1955 paper was published posthu- Henslowia Bl. (1850), p.p.
mously. The extensive use he made of fruit char- Hylomyza Danser (1940).
acteristics requires confirmation with modern
anatomical methods, using a greater selection of Glabrous parasitic plants on tree branches,
species. Perhaps more importantly, there is a stems neither twining nor bearing epicortical
need for detailed field observations on the events roots or secondary haustoria. Leaves expanded,
leading to germination and initial establishment alternate, base acute, apex rounded. Dioecious,
on the host (as there is for Dufrenoya), as well as the flowers small. Male inflorescence a (some-
the mature mode of parasitism (twining vs. non- times compound) umbel with one terminal and
twining, epicortical roots, secondary haustoria). several lateral flowers, the peduncle with scale
The above description is an amalgam of informa- leaves, those of the upper and lower part form-
tion from the two genera. ing an involucre. Staminate flower with 5 deltoid
At least some species show dimorphism in petals and 5 stamens inserted below them; disk
branches, a twining type of branches being squa- 5-lobed, flat. Pistillate flowers solitary, sessile,
mate and bearing haustoria, and a second type the peduncle similar to the staminate one;
being non-twining and leafy, mostly without ovary inferior; petals 5, deltoid, with 5 sterile
haustoria; this is a remarkable parallel to Cuscuta stamens inserted below them; disk 5-lobed, flat;
(Convolvulaceae; see Kuijt 1969). style short; stigma with 5 slender, spreading
There are some isolated items of information lobes. Fruit a drupe, petals persistent; mesocarp
that merit inclusion. van Steenis (1933) claimed with radially aligned, membranous fibers. Seed
that Dendrotrophe umbellata is non-parasitic, a sometimes furrowed longitudinally; embryo
view doubted by Danser (1940). Hambali (1977) with 5 parallel ridges that extend both upwards
later stated that the species is parasitic on nearby and downwards.
epiphytes, and that at maturity it produces thick Perhaps 11 spp., Thailand, Malaysia, and
branches that may also parasitize the branches of Indonesia.
the supporting tree.
13. Exocarpos Labill. Figs. 52–54
The seedlings of Cladomyza dendromyzoides
Stauffer become attached to the host branch, Exocarpos Labill., Rel. Voy. Rech. Pérouse 1: 155. 1798,
where it produces a sinuous radicle that follows nom. cons. # 2097; Stauffer, Mitteil. Bot. Mus. Univers.
host contours (Kuijt 1990). In C. cuneata, the Z€
urich 213: 1–260, tab. 4–20 (1959), rev.
endosperm is deeply lobed and contains a minute Sarcopus Gagnepain (1946).
embryo of a broadly fusiform shape, extending Sarcopodaceae Gagnepain (1947).
into two distinct, narrow cotyledons. Dendro- Sarcopodales Lam (1948).
myza reinwardtiana seeds have elongated, acicu-
lar, fibrous vascular bundles from the ovary wall Woody plants variable in stature, mostly gla-
that appear to provide an attachment mechanism brous, ranging from dwarf shrubs to trees 20 m
to the host, comparable to viscin. Its two cotyle- high, semiparasitic; lateral roots with numerous
dons, still recognizable by the shallow grooves haustoria, at times generating shoots; internodes
delimiting them, are completely connate. The variable in shape, terete, angular, or flattened into
conclusion must be that Cladomyza and Dendro- phylloclades. Leaves alternate, distichous when
myza are cryptocotylar in germination. The great with phylloclades, rarely paired, at times reduced
reduction of the radicular pole, in turn, suggests to scales in flowering areas, often heterophyllous.
(but does not prove) the formation of a primary Flowers bisexual or unisexual when sterile organs
haustorium as well as subsequent shoot produc- of the opposite sex present; sex distribution often
tion from the endophyte. Dendrotrophe stems not clear. Inflorescences diverse, essentially
generate many epicortical roots bearing second- spike-like, sometimes compound, when small
ary haustoria. often condensed in leaf axils, when terminal
Fig. 53. Santalaceae. Exocarpos neo-caledonica. A Young

axis. B Flowering phylloclade. C Inflorescence. D Ferti-
lized flower, longitudinal section. E Stamen. F Very young
fruit. G Mature fruit with pedicellar cupule. H Endocarp.
(Stauffer 1959, drawn by L.-M. Stauffer-Imhoof)
dorsi-basifixed, the 4 locules dehiscing longitudi-

nally; post-staminal hairs lacking; pollen tricol-
porate, barrel-shaped; glandular disk with short
lobes alternating with the petals, united with the
ovary; ovary mostly semi-inferior, the distinct
part conical, stigmatic lobes usually alternating
Fig. 52. Santalaceae. Exocarpos menziesii. A Flowering
shoot. B Leaves. C Inflorescence. D Flower, seen from with petals; ovary 1-chambered, placenta a cen-
above. E Branchlet with mature fruit. F Endocarp. G tral cone lacking differentiated ovules, embryo
Seed, longitudinally sectioned. (Stauffer 1959, drawn by sacs developing in the apex of the placental
L.-M. Stauffer-Imhoof) cone. Fruit superior to semi-inferior; base of
fruit encased by the greatly expanded, red pedi-
with basal bracts, or axillary, rarely reduced to a cel. Embryo dicotylous. n¼10.
single flower. Flowers small to minute, often in Twenty-six spp., many variable, Annam and
depressions on the axis, sessile or rarely short- E Java through Indonesia to New Caledonia, Aus-
pedicellate; petals 3–8, mostly glabrous on both tralia, Tasmania, New Zealand, and many South
sides but sometimes pilose, deltoid to oval; Pacific Islands, including Hawai’i.
stamens isomerous, opposite and basally It has been reported (Lam 1945) that E. pullei
attached to the petals, filaments very short, is both a stem and a root parasite, but this needs
156 Santalaceae
had come to realize that the subject was a known

species of Exocarpos, E. pullei Pilger.
14. Geocaulon Fernald
Geocaulon Fernald, Rhodora 30: 23 (1928).
Slender, unbranched, rhizomatous perennials to

30 cm tall. Leaves alternate, ovate, thin, apex
rounded, petiole short, venation evident. Flowers
in axillary clusters of 3, the central one bisexual
or pistillate, the two lateral ones functionally
male; petals 5, reddish, spreading; anthers as
many as the petals and opposite them; basal
disk somewhat lobed; filaments broad, scarcely
exceeding the lobes of the disk; anthers distinct
from the sepals; post-staminal hairs present;
ovarian cavity simple. Fruit a one-seeded drupe,
orange-red, the exocarp juicy. n¼13.
One sp., Geocaulon lividum Fernald, boreal
forest from the Atlantic to Alaska, Canada’s
Northwest Territories, and the B.C. coast, where
rare.
Sex distribution in Geocaulon remains
uncertain. The protologue (Fernald 1928) states
the central one (rarely two) flowers to be bisex-
ual, “the lateral mostly staminate and promptly
dropping after anthesis, or sometimes all the
flowers staminate”. Smith and Smith (1943)
write that the central flowers are pistillate and
the lateral ones staminate, representing
monoecy.
15. Jodina Hook. & Arnott Fig. 55
Fig. 54. Santalaceae. Exocarpos latifolia. A Flowering Jodina Hook. & Arnott, Hook. Bot. Miscell. 3: 172 (1833).
branch. B Leaf base. C Two spikes. D Pistillate flower
with lobed disk. E Petal with stamen. F Median section
of staminate flower showing pistillodium. G Bisexual Much-branched shrubs or small trees to 4 m high,
flower. H Fruit attached to swollen pedicel. (Koorders with alternate, rhombic, glabrous, stiff leaves,
and Valeton 1914, drawn by M. Mangoendimedjo) with one spine on each side and one at the apex;
base of leaf cuneate, petiole essentially lacking.
confirmation (see the introduction to Santalales). Inflorescence one or several small, pedunculate,
As mentioned previously, the genus Exocarpos axillary clusters of 7 or 8 flowers, with pubescent
was at the center of a curious error of interpreta- bracts. Flowers bisexual, lacking a calyculus;
tion that had unusual nomenclatural conse- petals 4 or 5, abaxially densely pubescent, adaxi-
quences. Impressed by what they thought was a ally glabrous except for a large post-staminal tuft
basically gymnospermous position of the ovules, of hairs; stamens as many as the petals, united
Gagnepain and Boureau (1947) described Sarco- with them at their very base; anthers dorsifixed,
carpus aberrans Gagn., and even the Sarcopoda- with 2 elongated locules dehiscing with a com-
ceae Gagn. One year later, Lam (1948) erected the mon longitudinal slit, filament short and stout;
Sarcopodales on that foundation, even though he ovary eventually inferior, with stout style, stigma
globular, grooved, 1-seeded drupe, bearing the

persistent petals; exocarp fleshy, endocarp stony;
embryo dicotylous.
Four spp., Canary Islands.
17. Leptomeria R. Br.
Leptomeria R. Br., Prodr. Fl. Nov. Holl. 1: 353 (1810).
Small shrubs, often much branched at the base, or

shoots terminating in thorns, internodes strongly
striate. Leaves squamate, alternate, usually
dropping soon, if persistent acicular to obovate.
Flowers either solitary in axillary positions or,
Fig. 55. Santalaceae. Jodina rhombifolia. A Flowering more commonly, in numerous, short, axillary
branch. B Flower, longitudinal section. C Mature fruit. D spikes; floral bracts persistent or caducous. Flow-
Same, longitudinally sectioned. E Embryo. (Pilger 1935)
ers very small, apparently always bisexual, sessile
or short-pedicellate; petals 5, spreading, thick,
blunt, weakly 3-lobed; ovarian cavity simple, with somewhat thickened and incurved apically; glan-
greatly contorted funiculus apically bearing 3 dular disk incised to lobed; stamens as many as
pendent ovules; glandular disk with large, dark the petals, opposite and basally united with them,
green colored, erect lobes alternating with the minute; filaments nearly lacking; anthers with 4
petals; receptacle broad. Fruit globular, drupe- locules facing inwardly and forming a circle; style
like, exocarp fleshy, rugose, pilose, divided into and stigma minute, the latter weakly lobed; ovary
5 longitudinal parts easily separating at maturity; inferior, top-shaped; ovarian cavity simple,
endocarp stony, sometimes splitting into 2 or 3 ovules not clearly distinct from the central pla-
parts. Seed solitary, globular, embryo ellipsoid, centa. Fruit ellipsoid-globular, with persistent
with two strap-shaped cotyledons. petals; exocarp thin, coriaceous, or juicy, endo-
One sp., Jodina rhombifolia Hook. & Arnott, carp thin, fragile; embryo very small.
S Brazil, S Bolivia, C Chile, Argentina S to Rı́o Seventeen spp., Australia and Tasmania.
Negro, Paraguay, and Uruguay.
18. Mida A. Cunn. ex Endl.
16. Kunkeliella Stearn
Mida A. Cunn. ex Endl., Gen. Pl. 5: 327 (1837).
Kunkeliella Stearn, Cuad. Bot. Canar. 16: 11–26 (1972). Santalum sect. Mida A. DC. in DC., Prodr. 14: 686 (1857).
Virgate, squamate, erect, shrubby root parasites, Small tree to 8 m high or shrub with mostly
branching sympodial. Leaf scales triangular, alter- alternate, shiny, lanceolate to obovate leaves.
nate. Inflorescence spike-like, with sterile bracts Inflorescence a small terminal or axillary, few-
below, few-flowered. Flowers bisexual, small to flowered panicle or raceme with up to 6 flowers.
minute, each subtended by a bract and two large, Flowers bisexual, mostly 5-merous (Cheeseman
acute prophyllar bracteoles; petals 5, spreading, 1914); receptacle lacking a calyculus; petals ovate,
not articulate from the receptacle, post-staminal constricted at the base; glandular disk with short,
hairs present; stamens as many as the petals, broad lobes between the petals; ovary semi-infe-
attached to the glandular disk where continuous rior; ovules 2 or 3. Fruit top-shaped, bright red,
with the petal bases; anthers biloculate, dehiscing apex nearly truncate.
with longitudinal slits, filaments short, basifixed; One sp., Mida salicifolia A. Cunn., New Zeal-
pollen prolate, 3-colporate, smooth, with alveolate and (North Island); extinct on Juan Fernández
faces; ovary inferior, unilocular; ovules 3, pendent Islands, as Santalum fernandezianum Phil. or
from the twisted central funiculus; style short, Mida fernandeziana (Phil.) Sprague & Sum-
stigma truncate, entire, capitate. Fruit a small, merh.
158 Santalaceae
Small, creeping, branched herbs, spreading by

means of slender stolons, with narrowly linear
or acicular, alternate leaves. Flowers small, in
groups of three in axils of upper leaves, bisexual;
calyculus absent (Dawson 1944); petals 4,
stamens 4, opposite petals, filaments very short,
locules 4, ovoid, dehiscing with a common slit;
post-staminal hairs present; glandular disk con-
cave, with short lobes between the petals; ovary
inferior, top-shaped; style short, stout, stigma
nearly spherical, weakly 2-lobed; ovarian cavity
simple, with 2 ovules pendent from the central,
short funiculus. Fruit a drupe, globular, red, exo-
carp fleshy, endocarp stony; embryo with 2 very
small cotyledons.
One sp., Nanodea muscosa Gaertn. f., extreme
South America, Staten and Falkland Islands. Pol-
lination is by small flies (Skottsberg 1901–1903,
p. 51).
21. Nestronia Raf.

Fig. 56. Santalaceae. Nanodea muscosa. Fruiting plant
from Sphagnum bog in Tierra de Fuego. (x 1.5, from
Kuijt 1969, drawn by author) Nestronia Raf., New Fl. Amer. 3: 12 (1836).
19. Myoschilos Ruiz & Pav.

Small, branching, glabrous, rhizomatous shrub to
a meter high, hemiparasitic; leaves paired, lance-
Myoschilos Ruiz & Pav., Fl. Peruv. Chil. Prodr.: 41, t. 34 olate. Dioecious, or flowers bisexual. Male inflo-
(1794). rescence an axillary, pedunculate umbel with
3–10 flowers lacking aborted style; pistillate flow-
Small, glabrous shrubs; leaves alternate, ovate to ers solitary, axillary; all flowers with obconical,
oblong. Inflorescence catkin-like, with 1–2 cat- inferior ovary; calyculus absent; petals 4(5),
kins per leaf axil. Flowers sessile, bisexual, sub- spreading, acute, puberulent along the margins;
tended by bracts; petals 5; anthers 5, epipetalous, stamens 4(5), opposite, accompanied by post-
filaments thread-like; anthers essentially basi- staminal tuft of hairs; filament very short,
fixed, locules 4, ovoid, dehiscing introrsely with attached to base of petals; style conical at base,
a common slit; glandular disk prominent, flat; stigma with 4 short lobes. Fruit an ellipsoid, small
ovary inferior, top-shaped; style short, slender, drupe.
stigma with 2–5 perpendicular lobes; ovarian cav- One sp., Nestronia umbellula Raf., E United
ity simple, ovules 3–5, pendent from a central, States.
stout funiculus, facing upwards. Fruit a drupe 22. Okoubaka Pellegr. & Norm. Fig. 57
with persistent petals, and partly enveloped by
bracts. Seed globular, embryo cylindrical, dicoty- Okoubaka Pellegr. & Norm., Bull. Soc. Bot. France 93: 139
lous. (1946).
One sp., Myoschilos oblongus Ruı́z & Pavón, S
Argentina and adjacent Chile. Tree to 40 m in height, its wood with sparse, wide
vessel elements with simple perforations; new
20. Nanodea Banks ex C.F. Gaertner Fig. 56 branches pubescent. Leaves alternate, short-peti-
olate, covered with simple hairs below, becoming
Nanodea Banks ex C.F. Gaertner, Fruct. 3: 251, t. 225 glabrous. Panicles many-flowered, with stellate
(1805). hairs. Flowers sessile, small, stellate-pubescent,
cially for such purposes. Parasitism in Okoubaka

has been documented by Swaine and Hall (1986),
and by Veenendaal et al. (1996). The seed is the
largest of any parasitic angiosperm (dry mass of
43 g).
23. Omphacomeria (Endl.) A. DC.
Omphacomeria (Endl.) A. DC. in DC., Prodr. 14: 680

(1857).
Broom-like shrubs with scale-like, alternate,

caducous leaves. Monoecious, flowers very
small. Staminate flowers sessile, crowded in
short axillary spikes, 4–6 at the tip of a thick
peduncle, the mostly 4 petals ovate, spreading;
glandular disk flat, scarcely lobed; stamens very
small, filaments short, thick; anthers with 4 lon-
gitudinally dehiscing locules; aborted style very
small or scarcely developed. Pistillate flowers sol-
itary or in pairs, sessile, 5-merous, at the tip of a
short, thick peduncle, sterile stamens poorly
developed; style short, straight, stigma 2-lobed,
sessile. Fruit an ovoid drupe, exocarp fleshy,
endocarp stony.
One sp., Omphacomeria acerba (R. Br.) DC.,
SE Australia.
24. Osyridicarpos A. DC.
Osyridicarpos A. DC. in DC., Prodr. 14: 635 (1857).
Fig. 57. Santalaceae. Okoubaka aubrevillei var. glabres- Shrubby plants, some scandent, twigs thin, not
centifolia. A Tip of branch. B Inflorescence. C Flower bud.
D Anthetic flower. E Flower, longitudinally sectioned. F angular. Leaves alternate, lanceolate to ovate.
Petal with stamen. G Young endocarp. (Louis and Léo- Inflorescence a small, axillary, 3–7-flowered
nard 1948, drawn by J.M. Lerinckx) cyme, or flowers solitary, axillary. Flowers bisex-
ual, 5-merous, without prophylls; petals with hair
by abortion more or less unisexual; petals 5, val- cluster behind the stamens; stamens connate with
vate; stamens 5, opposite petals; disk massive; the base of petals; filament thin, short; glandular
ovary inferior, unilocular, with 3 ovules; style disk not clearly delimited; ovary inferior; ovules
short; stigma lobed. Fruit a drupe. Seed one, 2 or 3, pendent from the apex of a convoluted
ovoid; endosperm copious; embryo small. funiculus. Fruit nut-like, bearing the lower por-
One (2?) sp., Okoubaka aubrevillei Pellegr. & tion of the receptacle.
Norm., Ivory Coast and Gold Coast. Okoubaka, Six spp., South Africa and East Africa to Eri-
perhaps the largest tree of Santalales (if not of trea.
parasitic angiosperms generally), reputedly is an
allelopathic tree, causing the death of surround- 25. Osyris L.
ing vegetation; however, this effect may be the
result of extensive root parasitism. The tree has Osyris L., Sp. Pl.: 1022 (1753).
a long history of medicinal and symbolic use by
native people in West and parts of Central Africa, Dioecious shrubs or small trees, much branched;
and ground bark products are still sold commer- twigs angular. Leaves alternate, lanceolate to
160 Santalaceae
bracteoles, or sometimes terminal. Flowers uni-

sexual, plants monoecious (rarely dioecious?),
flowers sometimes bisexual. Petals mostly 4–8.
Staminate flowers with short, epipetalous
stamens, filaments very short and flat; anthers
with 4 locules facing inwards, dehiscing with lon-
gitudinal slits; post-staminal hairs lacking; glan-
dular disk flat; aborted style very small. Pistillate
flowers lacking sterile stamens; ovary inferior;
ovarian cavity simple, often 4–6-lobed, funiculus
central, columnar, with 3(4 or 5?) pendent, ateg-
mic ovules at the tip. Fruit an oblong drupe, bear-
ing the persistent petals, exocarp fleshy; endocarp
bony. Seed ellipsoid, apically 5-lobed; endosperm
Fig. 58. Santalaceae. Phacellaria fargesii, parasitic on strongly lobed, embryo minute, completely undif-
Taxillus sutchuensis. (From Kuijt 1969, drawn by author) ferentiated, implying cryptocotyly.
Six or seven spp., India and Malaysia to S
linear-lanceolate, evergreen, usually glabrous and
China.
coriaceous. Dioecious or polygamous. Petals 3 or
4, deltoid, calyculus absent. Staminate flowers in Although no study of the endophyte is extant,
axillary, few-flowered cymes or racemes; style it is clear that the latter must be greatly fragmen-
lacking; glandular disk prominent, flat; stamens ted, as in Arceuthobium; it is also probable, again
as many as petals, distinct or nearly so, with small as in Arceuthobium, that the seedling’s epicotyl
tufts of post-staminal hairs; anthers dorsifixed, 4- aborts and that, consequently, all shoots are pro-
loculate, dehiscing with longitudinal slits. duced from the endophyte. This, in turn, may
Bisexual or pistillate flowers essentially sessile, imply the formation of a primary haustorium,
solitary or in threes, mostly at the tip of small probably the only one in Santalaceae.
shoots; petals 3 or 4; glandular disk with short
marginal tips alternating with petals; style stout, 27. Pilgerina Z.S. Rogers, Nickrent & Malécot
stigma with 3 or 4 lobes; ovary inferior, narrowly
obconical, with a simple ovarian cavity; ovules 2–4, Pilgerina Z.S. Rogers, Nickrent & Malécot, Ann. Missouri
attached to the tip of a stout central funiculus, Bot. Gard. 95: 398–400 (2008).
erect. Fruit drupe-like, spherical or ovoid, 1-
seeded; petals persistent; exocarp somewhat fleshy, Shrubs or trees to 12 m high. Leaves alternate,
endocarp thin, stony; embryo dicotylous. n¼15, 20. glabrous, elliptic to lanceolate, petiolate, venation
Two spp., Mediterranean and tropical Africa pinnate. Inflorescence a (sub)terminal bracteate
to S China. raceme with 8–23 flowers, slightly puberulent to
nearly glabrous. Flowers bisexual, pedicellate,
26. Phacellaria Benth. Fig. 58 each subtended by a minute, often caducous
bract; calyx absent; petals (4)5(6), distinct;
Phacellaria Benth. in Benth. & Hook., Gen. Plant. 3: 229 stamens one opposite each petal and basally
(1880); Danser, Blumea 3: 212–235 (1939), rev. adnate with it, post-staminal hairs present;
anthers dorsi-basifixed, locules 4, dehiscing
Small, glabrous or short-tomentose, squamate, introrsely by longitudinal slits; glandular disk
simple or sparsely branched plants of Arceutho- fleshy, nearly circular, with slightly upturned
bium-like aspect, sprouting diffusely from the rim where alternating with petals; ovary semi-
stems of various genera of Loranthaceae (rarely inferior, the receptacle broad; ovarian cavity sim-
from Dendrotrophe) or Viscaceae; scale leaves ple; ovules 1–3, pendent from a straight, central
alternate. Flowers sessile in axils of scale leaves, funiculus; style very short to absent, stigma
singly or in small clusters, often in irregular lon- essentially sessile, with 3–5 short lobes. Fruit a
gitudinal groups above the axils and with minute 1-seeded, broadly globular, glabrous drupe,
petals persistent; exocarp fleshy, thin; mesocarp without stamen hairs; anthers basifixed; style
thin, stony, smooth or finely grooved; endocarp exceeding the floral tube; stigma capitate, with
papery. three short lobes; glandular disk fleshy, elevated,
One sp., P. madagascariensis Z. S. Rogers, ring-shaped to nearly cupulate; ovules 3, pendent
Nickr. & Malécot; endemic to Madagascar. Per- from a short, straight funiculus. Fruit a nutlet,
haps congeneric with Staufferia. enclosed by a sclerified envelope representing
the bract and prophyllar bracteoles.
28. Pyrularia Michx. A taxonomically complex genus of perhaps
20 spp., S Chile and Argentina into Peru. Quinch-
Pyrularia Mich., Fl. Bor. Amer. 2: 231 (1803). amalium continues to be utilized as a folk medi-
cine in southern Chile; I have seen it being
Shrubs to 5 m high, root parasites. Leaves thin, gathered in large clumps, and have observed it
linear, lanceolate, to broadly elliptical, puberulent for sale at a local market.
when young, glabrescent in age, alternate. Dioe- Molecular data led Nickrent et al. (2010) to
cious or polygamous. Male inflorescence a place Quinchamalium (and Arjona) in their
raceme, many-flowered; fertile racemes shorter Schoepfiaceae, a suggestion that is here not fol-
and with fewer flowers. Petals 5, ovate, tip acute, lowed, as explained further above.
with post-staminal hairs. Staminate flowers in
terminal, small, panicle-like groups, with short, 30. Rhoiacarpos A. DC.
obconical hypanthium; disk with 5 short, glandu-
lar lobes alternating with short stamens; anther Rhoiacarpos A. DC. in DC., Prodr. 14: 634 (1857).
locules elongate, dehiscing with a longitudinal
slit; sterile pistil present; glandular disk with evi- Shrub with quadrangular internodes when young;
dent lobes alternating with petals. Pistillate flower leaves paired, ovate. Inflorescence a small axillary
with small, aborted stamens and short filaments; or terminal cyme, 1–5-flowered. Flowers bisexual,
style short, stout; ovary top-shaped; stigma 5-merous; hair clusters behind the stamens; glan-
depressed-capitate; ovarian cavity simple, with dular disk with short, rounded lobes between the
few, erect ovules on twisted funiculus. Fruit pyri- petals; ovary inferior; ovules 5, pendent from the
form to nearly spherical, a drupe with thin exo- central funiculus. Fruit an ovoid to gobular, edi-
carp, petals persistent, mesocarp stony; embryo ble nut; petals persistent.
globular, dicotylous. One sp., Rhoiacarpos capensis (Harv.) A. DC.,
Two spp., one in the eastern United States S eastern South Africa.
to Georgia, the other one in tropical parts of the
Central and E Himalayas. 31. Santalum L. Fig. 59
29. Quinchamalium Molina Santalum L., Gen. Pl., ed. 2: 165 (1742).
Santalum sect. (Eu)Santalum L.
Quinchamalium Molina, Saggio Stor. Nat. Chile 151 Santalum sect. Hawaiiensia Skottsb., Proc. 4th Pac. Sci.
(1782), nom. gen. cons. #2120. Congress, Java 436 (1919).
Santalum sect. Polynesica Skottsb., Proc. 4th Pac. Sci.
Herbaceous plants, some with woody base, some Congress, Java, 437 (1919).
rhizomatous, with distinct flowering and sterile Mida sect. Eucarya Kuntze in Post & Kuntze, Lex. Gen.
shoots from the base, both unbranched. Leaves Phan.: 367 (1903).
acicular to linear, acute, alternate. Inflorescence a
terminal, often crowded spike or capitulum. Semiparasitic trees or shrubs, twigs terete when
Flowers bisexual, at least one species distylous, young. Leaves mostly paired, rarely whorled; leaf
5-merous, basally invested by an envelope con- blade ovate to lanceolate to linear. Inflorescence in
sisting of the fusion between the bract and two axillary or terminal panicles. Flowers bisexual, 4-
prophyllar bracteoles, their tips distinct; floral or 5-merous; hair clusters behind stamens; fila-
tube elongated, flowers yellowish, often becoming ments short; glandular disk with triangular to
reddish in age. Stamens bilocular, with short fila- lobed marginal extensions between petals; ovary
ments attached to the mouth of the floral tube, semi-inferior or inferior; style slender, stigma
162 Santalaceae
Fig. 60. Santalaceae. Scleropyrum wallichianum. A Twig.

B Inflorescence. C Flower, one perianth segment
removed. D Infructescence. (L.S.L. Chua 1996)
Fig. 59. Santalaceae. Santalum album. A Flowering branch. B
Flower. C Gynoecium. D Stamen, ventral view. E Same, dorsal led to the rise of the local monarchy; conse-
view. F Fruit. G Same, longitudinal section. (Koorders and Vale-
ton 1914, drawn by M. Mangoendimedjo) quently, some species have become very rare.
For more details, see the introduction to Santa-
lales. Mida fernandezianum, once regarded as a
4-lobed; ovules 2–4, at lower end of elongated species of Santalum, is extinct on the Juan Fer-
ovarian papilla. Fruit globular, nut-like, exocarp nández Islands after exploitation as a source of
fairly thin, hard, wrinkled; germination (at least in sandal oil, but occurs in New Zealand as M. sal-
S. album) cryptocotylar (Bhatnagar 1965). n¼10, icifolia.
20. Santalum album has become locally estab-
Nineteen spp., India, N and E Australia, SE lished in Florida; it has also been introduced
New Guinea, and on numerous islands in the into Madagascar (Cavaco and Keraudren 1955).
South Pacific, including Hawai’i (see Harbaugh
and Baldwin 2007). 32. Scleropyrum Arnott Fig. 60
Santalum album, the original source of the
distinctively fragrant sandalwood and sandal oil, Scleropyrum Arnott, Mag. Zool. Bot. 2: 549 (1838), nom.
is of controversial geographical origin (probably gen. conserv. # 2103.
India), but has been commercially important for
at least two thousand years. Hawaiian species Trees or shrubs, often with spines on trunks and
were greatly exploited for the Chinese trade, and branches, with simple hairs on leaves, young
stems, and inflorescences. Leaves large, alternate, A single sp., Spirogardnera rubescens Stauf-
coriaceous. Inflorescence a spike with solitary fer, W Australia. This may instead be a species of
flowers or small clusters of flowers at the nodes. Choretrum.
Plants dioecious or polygamous. Inflorescence
catkin-like, axillary, or racemose with short-ped- 34. Staufferia Z.S. Rogers, Nickrent & Malécot
icellate flowers; petals 4 or 5. Staminate flowers
with 4 or 5 epipetalous stamens; filaments short; Staufferia Z.S. Rogers, Nickrent & Malécot, Ann. Missouri
anthers with 4 locules, dehiscing with an oblique Bot. Gard. 95: 394–398 (2008).
slit; post-staminal hairs present; aborted style
small or lacking; glandular disk annular. Pistillate Trees or shrubs: Leaves alternate, estipulate,
flower with inferior ovary; style short and thick; entire. Inflorescences axillary, the male thyrsoid,
stigma broadly peltate, with dentate margin; 4–10-flowered, bracteate, pistillate not seen.
ovarian cavity simple, with 3 ovules pendent Dioecious. Petals 5, sessile; calyx absent, stami-
from the tip of a straight funicular column. Fruit nate flowers with 5 epipetalous stamens; anthers
a large drupe, ellipsoid to pyriform, exocarp dorsi-basifixed; glandular disk stellate, lobes
thick, fleshy, endocarp stony. Seed solitary, glob- alternating with petals; sterile style present;
ular, embryo dicotylous. ovary inferior, 1-locular; ovules 1–3, pendent
About six closely related spp., Sri Lanka and from straight funiculus; style very short or
India to New Guinea. absent; stigma subsessile, with 3–5 lobes. Fruit a
One of the earliest references to a species of drupe, obovoid, single-seeded; exocarp fleshy, 5-
this genus described it as parasitic (van Rheede segmented, segments alternating with densely
tot Draakenstein 1636), but this cannot be pubescent furrows; mesocarp stony, endocarp
regarded as a reliable observation, as also stated papery, very thin; endosperm copious.
later by Arnott (1838). Ironically, 350 years later, One sp., Staufferia capuronii Z.S. Rogers,
it was nevertheless shown to be a root parasite by Nickrent & Malécot, endemic to Madagascar. Per-
Nicolson et al. (1988). haps congeneric with Pilgerina.
It is possible that Staufferia is not dioecious,
33. Spirogardnera Stauffer contrary to what the authors write, but that the
flowers are bisexual. The authors have not seen
Spirogardnera Stauffer, Vierteljahrsschr. Naturforsch. the pistillate flowers, and do not indicate the sex
Gesellsch. Z€
urich 113: 305–309 (1968). of any of their illustrations. The “staminodes” in
their Fig. K and L could be withered stamens,
Small, glabrous, shrubby, sympodial root para- instead. This may indicate that Pilgerina and
sites with terete, rigid stems and alternate phyllo- Staufferia should be united generically.
taxy. Juvenile leaves linear, early caducous, adult
ones squamate. Inflorescence a terminal, mostly 35. Thesidium Sonder
indeterminate spike of spirally arranged clusters
of 3 or 4 flowers. Flowers bisexual, sessile, petals Thesidium Sonder, Flora 40: 364 (1857).
(4) 5, not articulated, cucullate, with post-stam-
inal hairs; stamens as many as the petals and Profusely branched, small shrubs or herbs with
united with the base of the petals, filaments wooden base. Leaves alternate, mostly scale-like.
short; anthers dorsifixed, 2- or 4-loculate; glandu- Dioecious. Inflorescence a spike with numerous
lar disk with conspicuous, truncate lobes alter- flowers, these solitary or in clusters of 3 in axillary
nating with the petals; ovary inferior; style very positions to scale leaves, or in terminal spikes.
short, 5-lobed; ovarian cavity 5-chambered Flowers 4(5)-merous, each with two prophylls,
below, simple above; ovules 5, pendent from those of the pistillate more prominent than
straight, central funiculus. Fruit a 1-seeded, ses- those of the staminate. Staminate flowers: petals
sile, ellipsoid drupe bearing the persistent, closed with a cluster of hairs behind the stamens, the
petals; exocarp thin, mesocarp fleshy, endocarp latter with short filaments; the style much
stony; embryo mostly dicotylous. reduced or absent. Pistillate flowers: ovary
164 Santalaceae
inferior, glandular disk not clearly delimited; Danser, B.H. 1939. A revision f the genus Phacellaria
ovules 2 or 3, suspended from the tip of a slender (Santalaceae). Blumea 3: 212–235, Pl. 3–12.
Danser, B.H. 1940. On some genera of Santalaceae Osyr-
funiculus. Fruit a small nut bearing the persistent ideae from the Malay Archipelago, mainly from New
petals. Guinea. Nova Guinea, N.S. 4: 133–150.
Seven spp., southwestern South Africa. Danser, B.H. 1955. Supplementary notes on the santalac-
eous genera Dendromyza and Cladomyza (with pic-
tures of these genera and Hylomyza). Nova Guinea,
36. Thesium L. N.S. 6: 261–277, Pl. 9–24.
Dawson, G. 1944. Las Santaláceas Argentinas. Rev. Mus de
Thesium L., Sp. Pl.: 207 (1753). la Plata, n.s. 6: 5–80, Pl. 1–8.
Austroamericium Hendrych (1963). Der, J., Nickrent, D.L. 2008. A molecular phylogeny of
Santalaceae (Santalales). Syst. Bot. 33: 107–116.
Dobbins, D.R., Kuijt, J. 1974. Anatomy and fine structure
Perennial (rarely annual) herbs, some species rhi- of the mistletoe haustorium (Phthirusa pyrifolia). I.
zomatous, many African species with somewhat Development of the young haustorium, II. Penetra-
woody basal stems, or small shrubs. Leaves small, tion attempts and formation of the gland. Amer. J.
Bot. 61: 535–543, 544–550.
scale-like to mostly linear, alternate. Inflores- Engler, A., Krause, K. 1935. Loranthaceae. In: Engler, A.,
cence a panicle, raceme or spike, or composed Harms, H., Die nat€ urlichen Pflanzenfamilien, ed. 2,
of 3- or more-flowered cymes, flowers bracteate, 16b: 98–203.
with or without prophyllar bracteoles. Flowers 4- Fernald, M.L. 1928. Geocaulon, a new genus of the Santa-
laceae. Rhodora 30: 21–24.
or 5-merous, bisexual, gamopetalous, the recep- Feuer, S.M. 1977. Pollen morphology and evolution in the
tacle sometimes elongated; petals sometimes Santalales, sens. str., a parasitic order of flowering
hairy adaxially, or at least with a cluster of hairs plants. Ph.D. Thesis, University of Massachusetts.
behind (or on the back of) each stamen; filaments Fineran, B.A. 1963. Studies on the root parasitism of
Exocarpus bidwillii Hook. f. III. Primary structure
short, adherent to petal tube at its distal end; of the haustorium. Phytomorphology 13: 42–54.
ovary inferior; ovules 2 or 3, pendent from the Fineran, B.A. 1964. Id., IV. Structure of the mature haus-
tip of a convoluted funiculus. Fruit a small nutlet torium. Phytomorphology 13: 249–267.
with conspicuous surface venation, petals persis- Gagnepain, F., Boureau, E. 1947. Une nouvelle famille de
Gymnospermes: les Sarcopodacées. Bull. Soc. Bot.
tent. n ¼ 6, 7, 8, 9, 12. France 93: 313–320.
More than 240 spp. (perhaps the largest genus Hambali, G. G. 1977. On mistletoe parasitism. Proc. 6th
in Santalales), especially species-rich in arid South Conf. Asian-Pacific Weed Sci. Soc., pp. 58–66.
Harbaugh, D.T., Baldwin, B.G. 2007. Phylogeny and bio-
and Central Africa (including Madagascar), reach- geography of the sandalwoods (Santalum, Santala-
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SW Australia, and one introduced in Montana. Amer. J. Bot. 94: 1028–1040.
H€urlimann, H., Stauffer, H.U. 1957. Santalales-Studien II.
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Schoepfiaceae
Schoepfiaceae Blume, Mus. Bot. 1: 175 (1850).
Glabrous, semi-parasitic shrubs or trees occasion- a more or less campanulate fashion, an inferior
ally to 10 m high. Leaves alternate, entire, petiolate, ovary bearing a fleshy disk, and clearly 3-lobed
venation pinnate. Inflorescence a short, axillary, stigmas.
few-flowered raceme with small persistent basal
bracts. Flowers bisexual, pedicellate; calyx or caly- MORPHOLOGICAL AND BIOLOGICAL NOTES. The basal
culus not recognizable or inconspicuous but one cup should not be confused with a calyx or caly-
bract and two prophylls united directly below the culus, as it is placed below the (inferior) ovary.
ovary to form a 3-toothed cup; petals (4)5(6), The weak heterostyly in the genus (Tomlin-
united for most of their length to form a cylindrical son 1974) does not signify that the brachstylous
to subcampanulate corolla, the limbs spreading or form is unisexual, as it may form fruits.
recurved at anthesis; stamens as many as the petals Pollen in Schoepfia is said to be morphologi-
and connate with them at the latter’s middle, oppo- cally isolated, being more or less tetrahedral and
site the petals, each associated with a post-staminal heteropolar, and shows resemblances to several
hair tuft; filaments as long as the ovoid, dorsifixed, santalaceous genera (Sleumer 1984).
biloculate anthers that are placed at the flower’s Parasitism by Schoepfia schreberi on the roots
mouth; ovary inferior, surmounted by a massive, of nearby plants in Florida and the Bahamas has
fleshy glandular disk and long, slender style termi- been demonstrated beyond a doubt (Werth and
nated by 3-lobed stigma, but ovarian cavity Baird 1979), and parasitism by all species may
extending into the glandular disk, simple above, be assumed. Ten host species from 8 different
3-loculate below, with one unitegmic ovule pen- families have been recorded for S. schreberi,
dant into each cavity from a central, slender, showing a lack of host specificity.
straight basal funiculus; style as long as the floral Both Arjona and Quinchamalium, on the
tube and with a distinct stigma (dolichostylous basis of apparently strong molecular data, were
plants) or with smaller stigma and not reaching placed in Schoepfiaceae by Nickrent et al. (2010),
the anthers (brachystylous plants). Fruit a drupe but they are here retained in Santalaceae for
clasped in the somewhat expanded, persistent reasons given further above.
basal cup, outer layer thin and fleshy, inner layer Only one genus:
stony or papery; cotyledons 2 or 3. n ¼ 12.
The family is based on the single, name- Schoepfia Schreb.
giving genus of terrestrial, parasitic shrubs and
can be recognized by the combination of bisexual Schoepfia Schreb., Gen.: 129 (1789); Sleumer, Fl. Neotr. 38:
flowers lacking a calyx or calyculus but supported 19–38 (1984), rev.
by a floral cup representing connate prophylls
and bract and petals connate most of the way in Description as for the family.
168 Schoepfiaceae
The genus comprises 23 spp., 19 of which are References

American (Mesoamerica, Caribbean, and South
America to SE Bolivia and SE Peru); 4 other spp. Nickrent, D.L., Malécot, V., Vidal-Russell, R., Der, J.P.
are from Asia/Malesia. The genus is divided into 2010. A revised classification of Santalales. Taxon
three sections. Sect. Codonium (Rohr ex Vahl) 59: 538–558.
Sleumer, H. 1984. Olacaceae. Flora Neotropica 38: 1–159.
Endl., if retained, should be called sect. Schoepfia, New York: Organiz. For Fl. Neotrop.
since it contains the generic type, S. schreberi Tomlinson, P.B. 1974. Breeding mechanisms in trees
Gmelin, and consists of the 19 American species, native to tropical Florida – a morphological assess-
the other two sections being in tropical and E ment. J. Arnold Arb. 55: 269–290.
Werth, C.R., Baird, W.V. 1979. Root parasitism in Schoep-
Asia. Sect. Euschoepfia Engl. would thus have to fia Schreb. (Olacaceae). Biotropica 11: 140–143.
be renamed, if considered appropriate.
Viscaceae
Viscaceae Batsch., Tab. Aff. Reg. Veg.: 240 (1802); Barlow, Brunonia 6: 25–57 (1983); Barlow, Flora
Males. I, 13: 403–442 (1997); Wiens in Polhill & Wiens, Mistletoes of Africa, Roy. Bot. Gard., Kew
(1998).
Phoradendraceae H. Karsten (1860).
Loranthaceae subfam. Viscoideae Engler, Nat. Pflanzenfam. III, 1: 177 (1889).
Arceuthobiaceae Tiegh. (1897).
Dendrophthoraceae Tiegh. (1898).
Ginalloaceae Tiegh. (1900).
Shrubby, brittle parasites on the branches of bium, which is restricted almost entirely to the
woody dicots or Gymnosperms, glabrous or Northern Hemisphere.
with various types of vesture. Haustorial organs
developed from the radicular apex only, epicorti- VEGETATIVE MORPHOLOGY AND ANATOMY. Viscaceae
cal roots lacking, the endophyte often ramifying are evergreen or squamate parasitic shrubs on
within host tissues, in Arceuthobium reaching the branches of coniferous or dicotyledonous woody
host’s apical meristem under certain conditions; plants. The haustorium is single, mostly frag-
secondary aerial shoots formed from the endo- menting within the host tissues, and developing
phyte in many cases, exclusively so in Arceutho- cortical strands just outside the host cambium,
bium, Phoradendron californicum, and possibly these strands often producing radial sinkers that
in P. perredactum. Leaves paired, petiolate become embedded in host xylem. Epicortical
to sessile, estipulate, thin to coriaceous, entire, roots (and therefore secondary haustoria) are
in many species squamate, in Arceuthobium and absent. Internodes are terete to flattened or
Korthalsella entirely so. Inflorescences determi- winged, successive ones sometimes separated by
nate (indeterminate in Phoradendreae), in an inconspicuous constriction. The leaves are
various simple or complex patterns, in P. perre- opposite, simple, paired, estipulate, and show
dactum and some other reduced species little variation except in size, outline, and thick-
emerging directly from the endophyte. Flowers ness; petioles may or may not be formed.
unisexual, small, in monoecious or dioecious pat- Arceuthobium and Korthalsella are entirely squa-
terns; petals commonly 3 or 4; sepals or calyculus mate, as are numerous species of Dendrophthora,
absent; anthers sessile on, or connate with, the Phoradendron, and Viscum. An important taxo-
petals, with 1, 2, 4, or numerous locules, consoli- nomic feature in Dendrophthora and Phoraden-
dated into a central synandrium in Korthalsella dron (much less so in Ginalloa and Notothixos) is
and some African Viscum; pistillate flower with a type of leaf dimorphism involving pairs of scale
very short style; ovules absent; ovarian cavity leaves that may occupy various positions on the
simple, with basal ovarian papilla containing plant. In the first two genera, these structures
2 or more embryo sacs, or ovary solid. Fruit a 1 (cataphylls) are common in numerous species of
(2)-seeded berry with green endosperm; cotyle- Dendrophthora and Phoradendron (the inflores-
dons 2, often minute. Seed surrounded by a mas- cence is always made up of scale leaves, the basal
sive layer of viscin. ones in many cases being sterile, others subtend-
A family of seven genera and perhaps 450 ing flowers). Cataphylls are most common at the
spp., the great majority in three genera (Den- base of lateral branches; in nearly all species
drophthora, Phoradendron, and Viscum), mostly north of Mexico, and a few elsewhere, they are
tropical or subtropical, the genera limited to absent. They occur in two types, basal and inter-
either the Old or the New World except Arceutho- calary cataphylls. The number of basal cataphylls
170 Viscaceae
on lateral shoots and inflorescences may be as in Viscum minimum (Olson and Kuijt 1985),
high as 10 pairs. Intercalary cataphylls may Korthalsella, and Phacellaria (Kuijt and Dong
occur as a single pair or as series of pairs. The 1989). In all three cases, normal sieve-tube mem-
former condition is exemplified by P. chrysocla- bers were demonstrated, and the general absence
don and P. piperoides, the latter by P. crassifo- of such cells in Arceuthobium thus does not simply
lium, where the higher cataphylls subtend appear to be the result of size reduction of plants.
inflorescences. Basal cataphylls must not be con- Nevertheless, further studies in Arceuthobium are
fused with prophylls that, in certain species, may needed to establish whether differentiated phloem
be very prominent and may eventually subtend exists in the older portions of other large species.
lateral axes or inflorescences. They are very We also need to know the structural details of
inconspicuous in Ginalloa and Notothixos. For a A. globosum phloem as well as the tissues that in
description of leaf anatomy of Phoradendron, see other species occupy its position.
Gómez-Sánchez et al. (2011) and Dettke and
Milaneze-Gutierre (2007). BRANCHING PATTERNS. Aside from the actual struc-
ture of the inflorescences of Viscaceae, their posi-
STELAR ANATOMY. The tissue arrangement in the tion on the plant often bears an essential
stem of Viscaceae consists generally of a normal relationship to the branching patterns of the
siphonostele. No interfascicular cambium devel- plant as a whole. As in most mistletoes, the
ops in the secondary xylem of Arceuthobium majority of species in the family show a standard
(Wilson and Calvin 1996), the vascular bundles percurrent growth pattern, with inflorescences in
remaining separate. In that genus, the differen- axillary positions. In some Phoradendron species,
tiated xylem consists of small vessel elements with however, this is somewhat altered by the occur-
simple perforations only. In Phoradendron, xylem rence, along an innovation, of one or more pairs
also consists predominantly of vessel members of intercalary cataphylls, at least the upper ones
with simple perforations (Calvin 1967; Ashworth subtending inflorescences (e.g., P. crassifolium).
and Dos Santos 1997). Protophloem fibers are The percurrent pattern undergoes a fundamental
present in both Arceuthobium and Phoradendron. change where the tip of the shoot is replaced by
A detailed description of stem anatomy is an inflorescence (e.g., P. craspedophyllum), from
provided for three Mexican and one Brazilian which follows a dichotomous habit. A simplifica-
Phoradendron species by Gómez-Sánchez et al. tion of this results in the innovation having only
(2011) and Dettke and Milaneze-Gutierre (2007). one long internode and one pair of leaves plus the
There has been some uncertainty about the terminal inflorescence, the axillary buds of the
presence of phloem in Arceuthobium. While foliage leaves eventually forming the next gener-
phloem is clearly present in other genera, its ation of innovations. The well-known, symmetri-
absence in Arceuthobium was recorded many cally forking habit of Viscum album (Fig. 61)
years ago. Calvin and Wilson (1996), however, exemplifies this pattern, but numerous approxi-
mention metaphloem sieve elements in A. globo- mations of it are found also in Phoradendron. In
sum, and warn that such elements are often Ginalloa the same pattern has been illustrated
ephemeral and difficult to diagnose in proto- (Danser 1931; Barlow 1997) but seems not to
phloem. In fact, in an earlier paper, Calvin et al. have been mentioned in the accompanying
(1984), using fluorescent techniques only, had texts. What is less known is the fact that in one
convincingly demonstrated that sieve-tube mem- species of Arceuthobium, A. americanum, an even
bers exist in that species, probably the largest further simplification has evolved, but only in the
species in the genus. Unfortunately, no indication male plant, the female having a simple spike
of size or position on the plant of the internodes (Kuijt 1970). The most common male innovation
studied was provided. The thickest, most basal of A. americanum has a single internode termi-
internodes of this species are up to 4 cm thick. nating in two leaf scales and a solitary terminal
The question thus remains whether the occurrence flower. The axillary buds of these leaf scales pro-
of phloem is simply correlated with internodal or duce new, identical innovations each following
plant size. Since there exist other minute mistletoe season. Where little or no damage occurs over
species in the order, this question was explored the years, the approximate age of the male plant
Viscaceae 171
in a distinct pattern), but in other species are

borne on specialized branches that can be identi-
fied as inflorescences; intermediates also occur in
some species.
INFLORESCENCE. The inflorescences of Arceutho-

bium and Korthalsella have been mentioned in
the previous section. In Viscum, the basic inflo-
rescence unit is most commonly a single inter-
node terminating in a pair of leaf scales—leaves
cradling one median, terminal flower and two
others axillary to the scale leaves. This 3-flowered
unit may be unisexual, or the middle flower may
be staminate and the others pistillate, or vice
versa (Kirkup et al. 2000). In other cases, a second
internode is added that terminates in a single
flower or a 3-flowered unit, again with a variable
sex distribution. Compound, branched units may
also exist, as do units with more than 3 flowers.
Fig. 61. Viscaceae. Viscum album. A Fruiting branch. B In dioecious species like V. album, the male
Pistillate inflorescence. C Staminate inflorescence. (Kuijt and female inflorescences are often structurally
1969, drawn by author)
different, a feature reminiscent of Arceuthobium
americanum. Ginalloa has terminal and axillary
can therefore be read off, counting internodes inflorescences, each being an elongated spike of
back to the base of the plant (the internodes decussate pairs of sessile triads or single flowers,
elongate slightly every year). The difference with variable sex distribution. In Notothixos,
between the inflorescence and the shoot is here inflorescences are terminal, constructed of one
reduced to a matter of semantics. The branching or more flabellate, pedunculate cymules that
system in A. americanum is therefore very differ- may be organized in a compound arrangement.
ent between the sexes. In many other species of Cymules have 3–13 flowers, maturation proceed-
the genus (e.g., A. campylopodum), a flabellate ing from the central flower outwards. As in Ginal-
branching pattern exists that appears to have no loa, there is some variation in sexual distribution.
equivalent in the rest of the family except in the In the two genera making up Phoradendreae
inflorescence units of Notothixos and Viscum (Dendrophthora and Phoradendron), we meet an
(Kirkup et al. 2000). inflorescence type that is possibly unique in the
Terminal inflorescences result in a dichoto- flowering plants. Unlike all other inflorescences
mous habit, but there exist numerous Phoraden- in the family, it is indeterminate. The peduncle
dron species in which innovations of a single may be simple or may bear to 11 pairs of basal
internode (ignoring the existence of basal cata- cataphylls. There may be a single or numerous
phylls) form one pair of foliage leaves, the shoot so-called fertile internodes. Flowers are arranged
apex then aborting instead of forming an inflo- in longitudinal series directly above each fertile
rescence. This pattern equally results in a dichot- bract; in some species the series consist of only a
omy. Such an aborting shoot apex may be visible single flower each, being placed in an axillary
as a little spur, as in P. harleyi and P. liesneria- position. More commonly, we find more flowers
num. There are also Phoradendron species that above each fertile bract, in one, two, or 3 (rarely
combine dichotomous and percurrent branching 5) longitudinal series; there is always one flower,
on the same plant. the oldest one, directly above the axil of the fertile
The distinction between shoot and inflores- scale leaf. Frequently, flowers (or later, fruits) are
cence is similarly somewhat nebulous in the partly immersed in the swollen inflorescence axis,
genus Korthalsella, where flowers may be individually or in long grooves; they always lack
crowded in the axils of scale leaves (apparently bracts or bracteoles. In the male inflorescence of a
172 Viscaceae
few northerly species of Phoradendron, excessive Viscum species (Schaeppi and Steindl 1945) is no
numbers of flowers may form, the seriation more than a slight bulge just below the petals.
becoming completely irregular and the entire The internal structure of Viscacean flowers
circumference of the inflorescence internode has not been dealt with satisfactorily in the litera-
being ensheathed in crowded flowers. The curi- ture except for some species of Korthalsella
ous Dendrophthora cryptantha and D. harlingii of and Viscum (Schaeppi and Steindl 1945) and
southern Ecuador and adjacent Peru have single Arceuthobium (Cohen 1970). In the latter genus,
fertile internodes in which the fertile internode there is a central ovarian papilla in which two
swells up to almost completely encase the mature embryo sacs develop. The same is true for
fruits, the fertile internode appearing like a com- Korthalsella dacrydii, but only in its earliest
pound fruit. stages; a complete fusion eventually occurs, oblit-
While inflorescences in Phoradendron are erating the distinction between ovarian papilla
generally borne on stems, those of the curious P. and the surrounding tissues. In K. opuntia, the
perredactum arise directly from the endophyte ovarian cavity and stylar canal remain more evi-
(Rzedowski and Calderón de R. 2011); this may dent for some time. In Viscum, the absence of an
also be said for the smallest species of Arceutho- ovarian cavity and papilla has been recorded in a
bium. number of species. The most convincing and
most detailed of these reports have been by Zaki
FLOWERS. Flowers in the family are morphologi- and Kuijt (1994, 1995) in the minute Viscum
cally very simple, which in the pistillate may be a minimum. In such species, the embryo sacs there-
prerequisite of the complex anatomy of the even- fore originate in the base of a solid flower.
tual fruit; they are unisexual throughout. The
ovary is inferior and lacks anything resembling PALYNOLOGY. Few detailed studies are available for
a calyculus. The perianth segments (petals) form the pollen of Viscaceae except for a number of
a single whorl, mostly of 3 or 4 members that are Viscum species (Feuer and Kuijt 1982), but what
triangular in shape, and may or may not persist is known shows a spheroidal to subprolate shape
on the fruit. Pistillate flowers have a very short with a more or less rounded equatorial outline;
style and capitate stigma. Staminate flowers some African Viscum species have a lobate out-
mostly have a central disk, the anthers being line. In Africa, the number of apertures ranges
sessile in the middle of the petals (Ginalloa with from 3 to 6, but elsewhere pollen of Viscaceae
very short filaments), and may consist of two is 3-aperturate. Pseudocolpi are known from
(Ginalloa, Phoradendron), one (Dendrophthora), both Arceuthobium and Viscum; ornamentation
or mostly four locules (Notothixos). Viscum has ranges from psilate to verrucate or more or less
sessile anthers that resemble a multiloculate echinate. No clear relationships exist between the
cushion, but in at least one African species the pollen of Viscaceae and Loranthaceae, but a num-
androecium may form a solid, central, variable, ber of characters are shared with Eremolepida-
multiloculate, extrorse synandrium (Kuijt et al. ceae.
1979). Korthalsella has evolved a distinctive
synandrium; its minute anthers are connate, POLLINATION. The syndrome of floral features in
dehiscing introrsely into a central cavity with a Viscaceae clearly points to pollination by small
single common pore. In Arceuthobium, finally, insects, but few if any detailed studies are avail-
the archesporium seems to consist of a continu- able. A claim has been made for a certain amount
ous, ring-like cavity opening with a more or less of wind pollination in Arceuthobium in the
circular slit. The seven genera have thus evolved United States (Player 1979; Coppola 1989) even
strikingly diverse androecial equipment. In con- though flower structure does not indicate it.
trast, the pistillate flower shows little variation
throughout the family, even though that of EMBRYOLOGY. Embryo sac development has
Arceuthobium has two extremely minute petal received a certain amount of attention in Visca-
remnants contrasting to the more deltoid, persis- ceae, but the results are equivocal. In the studies
tent, 3 or 4 petals of other genera. The calyculus on Arceuthobium species, there is agreement that
claimed to exist in the pistillate flowers of some an ovarian papilla exists in the base of an ovarian
Viscaceae 173
cavity, two straight embryo sacs developing in the the endosperm-embryo complex, adhering
papilla. Embryo sac development in the family tightly to it, and is said to make up 80–90 % of
originates within the papilla, with a small lateral the fruit in some Mexican Phoradendron species
caecum (Bhandari and Vohra 1983), and is vari- (Gómez-Sánchez et al. 2011). In contrast to at
ously reported to be of the tetrasporic Adoxa type least some Loranthaceae, it seems to consist of
(Jones and Gordon 1965) or the bisporic Allium only one cell type, i.e., greatly elongated, slender
type (Tainter 1968). In both Dendrophthora and cells with thick, spirally structured primary walls
Phoradendron (York 1913; Billings 1933), the (Gedalovich et al. 1988). The precise anatomical
morphological conditions are the same as in location of the nutrients important to avian dis-
Arceuthobium, but the two embryo sacs grow persers has not been established. Presumably, the
down into the base of the flower and curve viscin cells also contain nutrients that are impor-
around to extend upwards into the ovarian wall, tant to avian dispersers, as the parental birds may
each carrying the egg apparatus with them to be seen to feed the decorticated fruits to their
directly above the ovarian cavity. So far, the pro- young (see Fig. 4a in Calder 1983). Even though,
cess is comparable to what happens in Lorantha- because of the absence of ovules, we can techni-
ceae—but the embryo sacs do not enter the style, cally not speak of seeds, the combination endo-
fertilization occurring within the ovary wall or in sperm-embryo-viscin should be so regarded. One
the papilla itself. The TEM study of Viscum mini- embryo per seed is normal, but seeds with two
mum (Zaki and Kuijt 1994, 1995) revealed the viable embryos appear to be relatively common
monosporic Polygonum type of development, in Viscum album and perhaps in other Viscaceae.
5–8 embryo sacs developing in each flower; how- As mentioned above, there is a surprising
ever, occasional patterns via the Allium type were lack of information on fruit anatomy. It is thus
also observed. What is clear from the above impossible, for example, to provide a proper
reports is, first of all, that the number of embryo functional explanation for the remarkable explo-
sacs per flower gives no guidance as to the num- sive dehiscence of fruits in Arceuthobium, in
ber of original carpels in the Viscacean flower; which the minute, bullet-shaped seed may be
secondly, it appears that we must exercise caution shot away for 20 m or more. In nature, the
in using embryo sac developmental types as sys- Arceuthobium fruit recurves when mature and
tematics criteria, even in comparison with Lor- the seed is expelled upwards through its base.
anthaceae. Unfortunately, embryological events The effect of this is that younger infections are
have not been studied in the great majority of established in the higher crown of the tree, so that
Viscacean species; the only relevant work avail- its population tends to keep pace with the upward
able is that on the above three genera. No studies growth of the host. The fruits of at least some
are available for Ginalloa, Korthalsella, or Korthalsella species are also said to be explosive,
Notothixos. but lack the sophisticated features of Arceutho-
bium.
FRUIT AND SEED. As in other mistletoes, the fruit is While most mistletoe fruits have a smooth
a single-seeded berry of various sizes and colors, surface, there are some that bear numerous
white predominating. The fruit surface of some tubercles, as in some African Viscum species
species of Viscum and Phoradendron is tubercu- and the American Phoradendron mucronatum.
late or, in the latter, rarely covered with bristles, Even more striking is the bristly surface of some
but smooth in most species and genera. The seed Mexican Phoradendron fruits, as in P. robinsonii
is surrounded by abundant viscin; the embryo is (Kuijt 2003). Such surface modifications are likely
dicotylous, the cotyledons sometimes very small. to have an unrecognized function related to bird
Both endosperm and embryo are chlorophyllac- foraging.
eous. Fruit anatomy has not been adequately
recorded, and is complex and probably variable DISPERSAL. Except for the events described for
between genera. The epidermis is generally Arceuthobium and Korthalsella above, all other
heavily cutinized. Below the epidermis is an Viscacean fruits are dispersed by birds, as was
undefined layer (or layers) of parenchyma. The apparently known for Viscum album even at the
viscin layer may surround most or only part of time of Theophrastus in Ancient Greece. The bird
174 Viscaceae
cohorts responsible for dissemination, of course, 1986a), Tristerix aphyllus (Kuijt 1988), and Phor-
differ in different areas. In Western Europe and adendron californicum (Kuijt 1989). (Interest-
North America, various thrushes as well as waxw- ingly, all of these taxa are squamate inhabitants
ings are important disseminators; the silky of deserts; the santalaceous genus Phacellaria
flycatchers are the major disseminators for the may be suspected of having the same germination
desert mistletoe, Phoradendron californicum. pattern.) In Viscum minimum, we see a somewhat
However, surprisingly little documented infor- transitional situation in that, while the epicotyl
mation is available for the majority of Viscaceae; dies and most shoots are derived from the endo-
in all probability, most Viscaceae may be dis- phyte, some may also be produced by the hausto-
persed by any of several frugivorous bird species. rial disk. The intrusive organ in Viscaceae is
Remarkably, Steindl (1935) reported that the seed formed endogenously from the haustorial disk
of Viscum album is ejected no more than 3 min- or wedge and usually becomes fragmented upon
utes after it is ingested, and Docters van Leeuwen entry into the host, profusely so in Arceuthobium.
(1954) reported similar findings for Indonesian It is not certain that a gland is involved in the
birds. There was no difference in viability with emergence of the endogenous intrusive organ, as
seeds placed directly on branches in Steindl’s it is in Loranthaceae and certain other Santala-
work. lean families, although Schmid et al. (2011) indi-
Long-distance dispersal of Viscaceae, as in cate a cavity for Phoradendron californicum that
Loranthaceae, has not been documented directly, the authors refer to as a gland but which differs in
but is strongly suggested in several cases. Phor- crucial respects. An earlier study on Viscum min-
adendron piperoides on Cocos Island (Costa imum (Olson and Kuijt 1986) failed to locate a
Rica), P. bolleanum on Guadalupe Island (Mex- gland. The parasite in such cases may be exclu-
ico), and P. berteroanum on the Galapagos sively endophytic in the first 1–2 years of its life.
Islands (Ecuador) are the most convincing candi- All shoots are then of endophytic origin; a pri-
dates (Kuijt 2003). The extraordinary geographic mary shoot does not exist. The epicotyl of Viscum
distribution of the genus Korthalsella around minimum survives for some time but does not
the Pacific and Indian oceans is also difficult to differentiate further. Sprouting from the hausto-
explain except by invoking the past agency of rial disk, as in V. minimum, also occurs in the
birds. Other suggestive instances are Arceutho- hyperparasite Phthirusa hutchisonii (see under
bium bicarinatum on Hispaniola and A. azoricum Loranthaceae) as well as in the hyperparasitic
on the Azores. Phoradendron dipterum and its relatives (Kuijt
The complexity of bird-mistletoe relation- 2003), but a connection to that mode of life is
ships has been highlighted by Restrepo’s (1987) not obvious. In Arceuthobium, Phoradendron,
study of the dispersal ecology of several small- and Viscum, the growing radicle may bifurcate
flowered mistletoes in Colombia. The major (Thoday 1951; Kuijt 1969, his Fig. 22-28c).
results of that work include the fact that the vari-
ables comprise not only different mistletoe spe- THE HAUSTORIUM. The endophytic system of Vis-
cies and their characteristics, but also different caceae is of a fundamentally different organiza-
ways of handling the fruits by avian dissemination than that of other mistletoes. As stated
tors. above, it is derived exclusively from the trans-
formed radicular apex, i.e., there are no epicorti-
GERMINATION. Germination is initiated by the cal roots with secondary haustoria. In the genera
growth of the radicular pole of the embryo to that have had the endophyte scrutinized, it has
the host surface, where a small disk or wedge is a dimorphic character, as described below for
formed against the host surface; the two cotyle- Arceuthobium, Phoradendron, Viscum, and
dons are then withdrawn from the green endo- Korthalsella.
sperm except in Arceuthobium, where they are Even though no gland may differentiate, a
scarcely differentiated and remain in the endo- collapsed zone is usually present (Kuijt 1969, his
sperm, dying (with the radicle) upon penetration Fig. 7-3b). The actual contact epidermis does not
of host tissues. This is remarkably similar to the show the same elaboration seen at least in Passovia
germination pattern in Viscum minimum (Kuijt (Loranthaceae), even though the contact cells grow
Viscaceae 175
out in a digitate fashion in Phoradendron califor- In the first type, the infection remains localized,
nicum (Schmid et al. 2011). There is no doubt that innumerable shoots arising from the center of a
the intrusive organ is endogenous, as elsewhere in spindle-shaped swelling. In the other two types,
Santalales. There seem to be no repeated efforts to the parasite eventually induces a broom-like for-
gain host entry—as, for example, in Comandra mation in the host from which mistletoe shoots
(Santalaceae)—and consequently no multiple emerge. In one broom type, its central branches
clasping layers and collapsed zones. are much swollen, the endophyte being restricted
Upon entering host tissues, the young endo- to those parts. In the second type of broom, the
phyte first grows towards the host xylem. ultimate endophytic filaments have reached the
Although often stated in the literature, there is host’s apical meristem where they remain perma-
no convincing evidence that the endophyte pene- nently embedded, elongating synchronously with
trates that tissue. In the early stages (which are the host. Shoot emergence from the first (aniso-
not properly documented) the endophyte gives phasic) type of broom is irregular, but in the
rise to lateral processes that grow parallel to the second (isophasic) type it is to a large extent
host cambium but external to it; these are known predictable (Kuijt 1960; Lye 2006). In isophasic
as cortical strands. In at least the above four brooms, apical dominance has been suppressed,
Viscacean genera, cortical strands produce radial all host branches becoming physiologically
structures called sinkers that also grow towards equivalent. The resulting brooms, especially in
the host xylem and eventually become encased in the A. douglasii-Pseudotsuga menziesii combina-
new layers of it (Thoday 1951, 1956a, 1956b, 1958, tion, often reach several meters in diameter. The
1961 for Viscum album and others). Thus the other species in which isophasic parasitism has
endophyte of these genera has a decidedly dimor- been documented are (host species in brackets):
phic character; in P. californicum (and probably A. americanum (Pinus contorta, P. banksiana,
in the South American P. fragile; Rizzini 1950) P. ponderosa), A. minutissimum (Pinus wallichi-
even the sinker system itself is dimorphic, some ana), and A. pusillum (Picea spp.). Curiously, in
sinkers being uniseriate and made up of paren- the rare instances that these mistletoes become
chyma only, while others are more massive and established on uncongenial hosts, as in A. amer-
also contain vessel members that are often in icanum on Picea engelmannii, an anisophasic
contact with host xylem (Schmid et al. 2011). broom develops; the symptomatolgy has changed
The general configuration of the cortical system radically. Isophasic parasitism in Arceuthobium
of Phoradendron species shows significant diver- likely evolved independently more than once, as
sity, partly because of different host species suggested by its documented occurrence in both
involved (Kuijt 1964). In Arceuthobium, the tips subgenera and four sections recognized by Nickr-
of both sinkers and young cortical strands are ent et al. (2004). In addition to the remarkable
unicellular, divisions in older parts resulting in Mexican Phoradendron perredactum that has
more massive strands that eventually differenti- recently been described (Kuijt 2011; Rzedowski
ate some xylem. Aerial shoots frequently emerge and Calderón de R. 2011), parallels to this mode
from cortical strands in some species; this is of parasitic behavior have evolved independently
especially true for Arceuthobium, where all in some holoparasitic plants in Apodanthaceae
shoots are derived from the endophyte. The (Pilostyles haussknechtii) and Mitrastemonaceae
same seems to be the case for Phoradendron (Mitrastemon) (Kuijt 1960).
perredactum where (as might be said in Viscum In Korthalsella, finally, the endophyte
minimum and the smallest species of Arceutho- spreads out against the host xylem upon entering
bium) the emergent shoots are inflorescences. the branch (Thoday 1958). In so doing, it appears
The highly advanced genus Arceuthobium to separate the xylem from its cambium, even
has evolved a type of parasitism that is unique encasing the entire xylem body in some instances
in Santalales but for the extraordinary above- by forming a sheath or continuous girdle around
mentioned species of Phoradendron. There are it. However, subsequent cambial activity may
three distinct modes of parasitism in Arceutho- embed parts or all of the mistletoe endophyte,
bium, their expression in part depending upon which may then extend centrifugal shafts of tissue
each of the host taxon and the mistletoe species. followed by renewed lobes again separating the
176 Viscaceae
new host xylem from extraxylary tissues. In this and Bolivia to Alaska, only Arceuthobium reach-
genus, there appears to be an active, complex ing beyond Oregon; Arceuthobium extends from
competition between the two partners, leading tropical Mesoamerica (Belize, Honduras, San Sal-
to a great deal of fragmentation of the endophyte vador) north to Alaska in western North America,
and a complex, irregular mass of tissues of both and eastwards in Canada to the Atlantic coast,
partners. It is to be expected that different host with one isolated endemic on Hispaniola. In the
species respond variously. Old World, Viscum is widely distributed from
The interface between host and parasite Western Europe and the Mediterranean to Japan
tissues is predominantly parenchymatous but and Australia and has a strong representation
includes some open xylem-xylem contact. The in Africa; Arceuthobium is more limited, being
ultimate tips of cortical strands are probably known from southern France, the Iberian Penin-
always multicellular, except in Arceuthobium sula and NW Africa, with isolated occurrences in
(see above). The overall structure of the endo- East Africa and the Azores, and the Himalayan
phyte varies to some extent with host species; region to southern China. Korthalsella is found
on an uncongenial host, cortical strands may around the Indian and eastern Pacific Ocean
not (or only weakly) develop or even may be areas, from East Africa and Madagascar to
walled off by the local growth of host tissues in Japan, Hawai’i, New Zealand, and Australia. The
Phoradendron. The continuing secondary growth two small genera Ginalloa and Notothixos are
of the host, and the eventual transformation of its Indomalaysian and reach from Sri Lanka to Aus-
extraxylary tissues into cork, often exposes the tralia, respectively. Viscum album was introduced
cortical strands, which may become bright green, to the Santa Rosa area of California during the
and which in some species may generate more 1930s by the well-known American horticultural-
aerial shoots. Much local growth may result in ist Luther Burbank, and has spread significantly
massive swellings. The minute, South African V. (Scharpf and Hawksworth 1976).
minimum in nature is limited to two species of
fleshy Euphorbia, in which its endophyte ramifies PHYLOGENY AND RELATIONSHIPS WITHIN THE FAMILY.
freely (probably without forming sinkers) but The mutual phylogenetic relationships of Visca-
induces no swelling (Kuijt 1986a). cean genera remain obscure except for the very
close affinities between the American genera
CHROMOSOMES. The basic chromosome number in Phoradendron and Dendrophthora, which are
Viscaceae is n ¼ 14, but other numbers occur occasionally difficult to tell apart. The family is
(n ¼ 10, 11, 12, 13, 15, 20), probably indicating believed to be of Northern Hemisphere origin,
progressive reductions for most. Chromosomes possibly in eastern Asia, and the New World
tend to be among the largest in the plant king- ancestors of Phoradendreae and Arceuthobium
dom. Sex-associated and floating chromosome may have migrated across the Beringian land
translocation complexes have suggested a con- connection during the Tertiary.
nection with the origin and establishment of The present treatment does not follow APG
dioecy and subsequent secondary radiation in III (2009), where Viscaceae are embedded in San-
African Viscum (Wiens and Barlow 1975, 1979). talaceae. Nickrent et al. (2010) continue to recog-
The only known instance of polyploidy (tetra- nize the family, as I do, and consequently find it
ploidy) in the family is the Galapagos population necessary to split Santalaceae, s.l., into six sepa-
of Phoradendron berteroanum (Kuijt 2003). rate families. In my opinion, continued recogni-
tion of the Viscaceae as a family is warranted for a
HYBRIDIZATION. There are no convincing cases of number of reasons. Viscaceae have exclusively
intraspecific hybrids in Viscaceae; the two unisexual flowers; this is true only exceptionally
instances in Phoradendron referred to by Wiens in Santalaceae. All Viscaceae have paired phyllo-
and DeDecker (1972) have more acceptable taxy; only a very few Santalaceae do. Viscaceae
explanations (Kuijt 2003). are exclusively branch-parasitic; nearly all Santa-
laceae are terrestrial parasites. The entire hausto-
DISTRIBUTION. In the New World, including the rial system of Viscaceae is embedded within host
Caribbean, the family reaches from Argentina tissues; the (undocumented) absorptive system of
Viscaceae 177
Phacellaria forms the only Santalacean counter- outcome measures. See the summaries in Becker
part. Post-staminal hairs are typical of practically and Schmoll (1986), B€ ussing (2000), Kirkup et al.
all Santalaceae but unknown in Viscaceae. In all (2000), and the brief summary by Kaegi (1998).
but a couple of highly advanced Santalacean Religion and Mythology. Viscum album is the
genera, ovules are still recognizable, being sus- mythological plant par excellence, and its history
pended from a twisted, central funiculus, while in Western Europe is an interleaved mixture of
no ovules are present in Viscaceae, the embryo folklore and superstition with an occasional
sacs usually being contained within a small basal admixture of religion. It is especially in Great
papilla. The fruit of Viscaceae has a highly Britain that its status has survived and, by exten-
specialized tissue called viscin that has no equiv- sion, in other Anglo-Saxon countries, especially
alent in Santalaceae. Avian seed dispersal is the United States, where there happens to be a
unimportant in Santalaceae but absolutely essen- somewhat similar species of mistletoe in Phora-
tial in Viscaceae. Root caps on the radicle are dendron. As mentioned above, mistletoes were
present in Santalaceae, but not in Viscaceae. All known to ancient writers like Pliny (first century
these features warrant the continued recognition CE), but it is not certain whether this was Viscum
of Viscaceae as a clearly circumscribed, easily album or Loranthus europaeus. The ever-green-
recognizable taxonomic entity. ness of V. album early on seems to have given the
plant an aura of eternity, and its lack of contact
VISCACEAE AND HUMAN SOCIETY. Medicinal Aspects. with the earth was easily transmuted into divine
The earliest references to the medicinal use of status. Even Pliny refers to its use to guard against
mistletoe appear in Pliny’s writing, which refers evil spirits; in medieval times, rosaries out of
to the use of (probably) Viscum album by Gauls mistletoe wood were prized, and sprigs were
as a cure for sterility and epilepsy (Calder 1983). sometimes carried into battle. Its association
Some of the early medieval herbals also indicate with Christmas may be of a more recent vintage,
local medicinal uses of the plant. Culpeper’s later and a linear connection of this folkloristic rem-
herbal (1653, reprint 1995) reads that Misselto “is nant to the ritual use by Druidic priests is ques-
a cephalic and nervine medicine, useful for con- tionable. The Druidic ritual, as is well known, was
vulsive fits, palsi, and vertigo”, and also for “fall- focused on Viscum album on oaks, which is an
ing sickness”. Thus, it seems to have been exceedingly rare occurrence but, because of the
accepted as a “cure-all” plant in England and separate, highly sacred status of oaks, rendered
elsewhere in Western Europe. There are scattered its appearance on this tree particularly esteemed.
reports of other Viscum species used medicinally, It is not surprising that healing properties were
such as the Australian V. articulatum used for ascribed to V. album in many early herbals, and
stomach complaints and high blood pressure that the plant was said to protect one from vari-
(Watson 2011). Numerous instances of such ous diseases, from evil, from lightning, and from
applications are listed for various Phoradendron other natural disasters and accidents. It is also
species in my monograph (Kuijt 2003, Appendix tempting to speculate that the medicinal proper-
4). Hawksworth and Wiens (1996), similarly, list a ties ascribed to it by the German Rudolf Steiner
variety of very local uses for Arceuthobium. were ultimately rooted in such traditions. In
The German mystic and educator Rudolf Stei- many areas in contemporary Germany, the plant
ner in the early 20th century conceived of the idea is seen on local markets well into January; until
that the European mistletoe, Viscum album, con- fairly recently, the mistletoe was often included in
tains properties that are effective in the treatment New Year’s wishes and greetings. The Anglican
of cancer, and a minor industry based in Church in Great Britain, however, was uneasy
Germany to this day continues to produce such about the use of mistletoe and, until the late
medications. The literature on the subject is 19th century, banned the plant from its churches,
problematic and, regretfully, a more recent criti- considering its regard a Celtic, heretical remnant.
cal evaluation by qualified medical researchers of An extensive account of the history and mythol-
published clinical trials (Ernst et al. 2003) has ogy of V. album from ancient times to the present
concluded that none provide tangible improve- was published in Tubeuf (1923). Even today, in
ments in the quality of life, survival, or other Great Britain and much of the rest of Western
178 Viscaceae
Europe, V. album frequently enjoys an unspoken – Inflorescences determinate (not elongating), or flowers
local protection as a result of its historical and sessile in leaf axils or bracts, not arranged in longitudi-
mythological background. Some more recent nal series on inflorescence internodes; basal cataphylls
details for New England are provided by Howard absent (present in Ginalloa and Notothixos) 3
2. Anthers unilocular; flowers uniseriate in many, but not
and Wood (1955) for Phoradendron leucarpum.
all, species 2. Dendrophthora
Viscum album has frequently been used as a – Anthers bilocular; flowers only exceptionally uniseri-
motif in the decoration of ceramics, glassware, ate, usually 2- or 3-seriate 6. Phoradendron
jewelry, and other luxury items in Europe (see 3. Plants squamate 4
Becker and Schmoll 1986). – Plants foliaceous 6
Economic Aspects. Many Viscaceae seriously 4. Parasitic on Pinaceae and Cupressaceae only; anther
damage the host tree, resulting in disfigured with ring-shaped archesporium 1. Arceuthobium
branches or trunks, and inevitably leading to – Parasitic on dicotylous woody plants or Podocarpa-
lessened vigor and life span. Plants of Viscum ceae; anthers otherwise 5
album in northern France and in Germany, for 5. Staminate flowers with a central synangium with com-
example, are very obvious in deciduous hosts mon terminal pore 4. Korthalsella
– Anthers cushion-like on petals, with several to many
during the winter, and often no efforts are made
separate, small pollen sacs, rarely connate into a cen-
to remove them. However, their damage does not tral cone 7. Viscum
compare to the effects of dwarf mistletoe parasit- 6. Plants densely covered with branched hairs, white to
ism. golden or brownish 5. Notothixos
The genus Arceuthobium contains some of – Plants glabrous or nearly so, green 7
the world’s most serious forest pathogens. The 7. Inflorescence an elongated spike with decussate pairs
damage consists of three major categories. of single flowers or very short 3-flowered cymes;
There is, first of all, the decreased growth rate of anthers opening with slits 3. Ginalloa
the affected host, conditioned by the size of the – Inflorescence a 3- or 5-flowered cyme; anthers cushion-
tree and the number and size of the mistletoes it like or united into a central synandrium, poricidal
bears. Secondly, parasitism by Arceuthobium fre- 7. Viscum
quently involves—depending upon the particular
host-parasite combination—severe malforma-
tions on the tree that significantly reduce its GENERA OF VISCACEAE
commercial value. The most striking and impor-
tant of these are the various types of witches’ 1. Arceuthobium M. Bieb. Fig. 62
brooms involving localized heavy swellings and/
or excessive proliferation of parasitized branches. Arceuthobium M. Bieb., Fl. Taur.-Caucas., Suppl. 629.
Thirdly, especially in the case of older Arceutho- 1819, nom. gen. conserv. # 2091; Kuijt, Mem. Torrey
Bot. Club 22: 1–38 (1970), rev.; Hawksworth & Wiens, U.
bium infections, local wounds often develop in
S. Dept. Agr. Handb. 709: i–xiv, 1–410 (1996); Nickrent
consequences of the action of fungi or insects that et al., Amer. J. Bot. 9: 125–138 (2004), rev.
are attracted to the endophytic parts of the para-
site and/or the malformations caused by it. In the Squamate plants, usually small, parasitic on Pina-
Pacific Northwest, the resulting commercial dam- ceae (New World) and Pinaceae or Cupressaceae
age is believed to exceed that of any other single (Old World), yellowish green to reddish brown or
cause. bright green, the scale leaves paired; plants rarely
to 40 cm in size, one sp. no more than 4 mm,
larger ones profusely branched; endophyte
KEY TO THE GENERA OF VISCACEAE greatly fragmented, in certain cases reaching far
into host tissues and inducing types of brooming
1. Inflorescence a (frequently elongating), indeterminate of the host, especially where apical meristems are
spike of one or more fertile internodes, each fertile invaded; shoot production from the endophyte
bract subtending 1–many flowers above it on the axis, only, the epicotyl withering. Dioecious. Inflores-
in longitudinal series; basal cataphylls on lateral cence a spike or, at least mostly in male A. amer-
branches of many, but not all, species 2 icanum, a simple, one-flowered unit that repeats
GENERA OF VISCACEAE 179
Fig. 62. Viscaceae. Arceuthobium azoricum. A Plant that

has induced a thickening at the end of the host branch. B
Distal portion of pistillate shoot showing verticillate,
nearly mature fruits. C Distal portion of staminate shoot
showing flowers in anthesis. (Hawksworth and Wiens
1975)
itself annually in dichasial fashion. Staminate

flower (2)3–4-merous, sessile; the sessile anther
cushion-like; pollen cavity circular and dehiscing
with a circular slit; pistillate flower ovoid, with
2 minute perianth members flanking a small
stigma. Fruit an ellipsoid, one-seeded berry that,
when ripe, explodes in all but one sp., the small, Fig. 63. Viscaceae. Dendrophthora obliqua. A Habit. B
bullet-shaped seed and viscin escaping through Staminate inflorescence. C Pistillate inflorescence. D Petal
the upturned base. n ¼ 14. and anther. E Fruit. (Kuijt 1986b, drawn by author)
Forty-two spp. (according to Nickrent et al.
2004); one sp. on Hispaniola, and one on the 2. Dendrophthora Eichler Fig. 63
Azores; various spp. from Belize, Honduras, and
San Salvador into northwestern America to Dendrophthora Eichler in Mart., Fl. Brasil. 5(2): 102
Alaska, with one sp. reaching through Canada (1868); Kuijt, Wentia 6: 1–145 (1961); Kuijt, Bot. Jahrb.
from Saskatchewan to the Atlantic coast and Syst. 122: 169–193 (2000); Kuijt, Novon 21: 444–462
into nearby New England; one sp. ranging from (2011), rev.
the western Mediterranean (including Morocco
and Algeria) to the Middle East and the Hima- Plants leafy or squamate, green; phyllotaxy decus-
layas of India, Pakistan, and China; other species sate (one Caribbean sp. 3-whorled), glabrous or,
in Mexico, southern China and Eritrea, Ethiopia, very rarely, short-pilose; internodes terete, flat-
and Kenya; an extremely small sp. in the southern tened, or quadrangular; haustorial attachment
Himalayas (India, Nepal, Bhutan, Pakistan). simple; epicortical roots lacking; vegetative
180 Viscaceae
reproduction from the endophyte rare; plants

parasitic almost exclusively on stems of woody
dicots, rarely on Gymnoperms. Branching per-
current, rarely dichotomous through terminal
abortion or terminal inflorescences. Leaves thin
or fleshy, cataphylls at the base of lateral stems
and/or inflorescences frequent. Dioecious or
monoecious. Inflorescences spike-like, squamate,
the base with one or more sterile internodes fol-
lowed by one or more fertile internodes bearing
partially sunken, sessile flowers in 1 or 3 (very
rarely, 2) longitudinal series. Staminate flowers
mostly 3-merous, petals deltoid, each bearing a
minute, sessile, unilocular anther; rudimentary
style small. Pistillate flower similar, without
anther rudiments. Berry mostly white or yellow-
ish. Seed solitary, with abundant viscin and green
endosperm; embryo with 2 minute cotyledons.
n ¼ 14.
At least 120 spp. in tropical America, from
southern Mexico to Bolivia and throughout the
Caribbean (where much endemism), mostly at
higher altitudes on the continent, but also lower
in the Caribbean. Frequently difficult to separate
from the much larger genus Phoradendron, which
has bilocular anthers rather than unilocular ones,
and only very rarely uniseriate flowers.
3. Ginalloa Korth. Fig. 64
Ginalloa Korth., Verhand. Bat. Genootsch. 17: 260 (1839);

Fig. 64. Viscaceae. Ginalloa flagellaris. A Habit. B Inflo-
Barlow, Fl. Mal. I, 13: 412–418 (1997).
rescence with two axillary flowers, each flanked by two
younger flower buds. (Barlow 1997, drawn by L. Spindler)
Glabrous, much-branched plants; internodes stri-
ate or longitudinally wrinkled. Leaves decussate, 4. Korthalsella Tiegh. Fig. 65
curvinerved with 1–5 prominent veins; lateral
branches with one pair of basal cataphylls, usu- Korthalsella Tiegh., Bull. Soc. Bot. France 43: 83, 163
ally well above the base. Monoecious. Inflores- (1896); Touw, Blumea 29: 525–545 (1984); Molvray,
cences terminal and axillary, each a spike of Novon 7: 268–273 (1997); Molvray et al., Amer. J. Bot.
decussate pairs of triads or single flowers, the 86: 249–260 (1999), rev.
median (or only) flower of a unit staminate, lat-
eral ones staminate or pistillate, with minute, Small, glabrous, squamate plants; internodes
fimbriate bracteoles. Staminate flowers terete or compressed to various degrees. Leaves
0.5–1 mm long, globose or somewhat flattened, decussate or distichous, reduced to minute
3-merous; anthers on short filaments, disk- scales. Perhaps all species monoecious. Inflores-
shaped, 2-loculate, opening by slits; pistillate cences small and few-flowered, sometimes spike-
flowers usually <2 mm long, cylindrical to nar- like, sometimes absent and the flowers axillary
rowly ellipsoid, usually 3-merous; stigma minute. in crowded clusters separated by multicellular
Fruit ellipsoid, smooth or tuberculate. hairs, occasionally surrounding the entire node.
Perhaps nine spp., Sri Lanka E and S to New Flowers minute, 3-merous, the first one in axil-
Guinea and Solomon Islands. lary position and usually staminate and later
GENERA OF VISCACEAE 181
Fig. 65. Viscaceae. A Korthalsella papuana. B K. rubra. C

K. geminata. D Same, part of inflorescence. (Barlow 1997)
ones pistillate, the staminate with central synan- Fig. 66. Viscaceae. Phoradendron madisonii. A Habit. B
drium with 3 pairs of introrse locules and a Inflorescence and infructescence; note the pairs of cata-
phylls at the base of the spikes and between the pairs of
common terminal pore. Berry pyriform to foliage leaves. (Kuijt 1986b, drawn by author)
ellipsoid, mostly <3 mm long, green, slightly
explosive in at least some species; cotyledons
rudimentary. n ¼ 14. flowers, the central one(s) staminate and matur-
Perhaps 15–25 spp., around the central and ing first, others pistillate and developing sequen-
western Pacific and Indian oceans, including E tially to the sides; staminate flowers globose, ca.
Africa, Madagascar, and New Zealand. 1 mm in diameter, short-stipitate, usually 4-mer-
5. Notothixos Oliver ous; anthers with short filaments, ovoid or reni-
form, multiloculate, locules opening by pores;
Notothixos Oliver, J. Linn. Soc. Bot. 7: 92, 103 (1864); pistillate flower cylindrical to barrel-shaped, usu-
Barlow, Brunonia 6: 1–24 (1984), rev. ally <2 mm long, 4-merous; stigma minute, nip-
ple-shaped. Fruit narrowly ellipsoid to nearly
Much-branched plants, densely tomentose on globose. n ¼ 12, 13.
young parts, creamy to light brown, lateral Eight spp., Sri Lanka E and S to E Australia
branches mostly with a pair of inconspicuous, and Santa Cruz Islands.
acute basal cataphylls above the axil; mono- 6. Phoradendron Nuttall Figs. 66, 67
ecious. Leaves decussate, curvinerved with 3
or 5 prominent veins. Inflorescences terminal, Phoradendron Nuttall, J. Acad. Nat. Sci. Philad. II, 1: 185
sometimes branched, the individual units fan- (1848); Kellogg & Howard, J. Arnold Arb. 67: 65–107
shaped and pedunculate, solitary or in racemose (1986); Kuijt, Syst. Bot. Monogr. 66: 1–643 (2003); Kuijt,
to spicate arrangement, each unit bearing 3–13 Novon 21: 444–462 (2011).
182 Viscaceae
variously shaped, petiolate or sessile; lateral

branches and inflorescences often subtended by
one or more pairs of cataphylls. Dioecious or
monoecious with diverse patterns of sex distri-
bution. Inflorescence spike-like, squamate, with
at least one basal sterile internode followed by 1
or more fertile ones along which the sessile, often
partially sunken flowers show diverse patterns of
longitudinal seriation. Staminate flowers with (2)
3(4) small, triangular petals each bearing a small,
sessile, bilocular anther; rudimentary style pres-
ent. Pollen tricolporate, isopolar. Pistillate flower
like the staminate; rudimentary anthers absent;
style short and straight, stigma undifferentiated;
ovary unilocular, with central ovarian papilla
producing at least 2 embryo sacs. Fruit a white,
or yellow to red berry, the single seed with
abundant viscin and green endosperm. Seedling
with two minute cotyledons, germination pha-
nerocotylar (cryptocotylar in P. californicum).
n ¼ 14 (28).
Closely related, and often difficult to sepa-
rate from Dendrophthora; presently with about
240 spp., reaching from eastern North America
and Oregon to Bolivia and Argentina, with
strong representation but little endemism in
the Caribbean area; in continental areas, it
tends to be limited to lower and middle eleva-
tions.
The curious Phoradendron perredactum from
Oaxaca deserves special mention, as it is the only
known species in the genus that has evolved iso-
Fig. 67. Viscaceae. Phoradendron canzacotoi. A Stami- phasic parasitism (Kuijt 2011; Rzedowski and
nate plant. B–D Same, details of branch tip, inflorescence, Calderón de R. 2011), and also because its inflor-
and staminate flower, respectively. E Infructescence.
(Kuijt 1986b, drawn by author) escences emerge directly from the endophyte.
7. Viscum L. Figs. 61, 68, 69
Small to moderately large plants, brittle, parasitic Viscum L., Sp. Pl.: 1023 (1753); Wiens in Barlow & Wiens,
on woody dicotyledons or gymnosperms, mostly Mistletoes of Africa. Royal Botanic Gardens, Kew (1998).
glabrous to short-hairy; epicortical roots lacking,
the host attachment simple, sometimes addi- Minute to large, branching, glabrous parasites of
tional shoots formed from within host tissues; woody dicotyledons (rarely Pinaceae), host
internodes terete, quadrangular, carinate or attachment single, or shoots sprouting from
compressed to various degrees. Branching per- within host tissues; internodes terete, quadrangu-
current, or dichotomous by terminal abortion or lar, or flattened; branching percurrent, dichoto-
terminal inflorescences. Leaves paired (one mous, or otherwise. Leaves decussate, variously
Mexican sp. 3-whorled), often somewhat fleshy, shaped, squamate in some species. Dioecious or
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Fig. 68. Viscaceae. Viscum loranthii, epiparasitic on

Scurrula ferruginea. (Danser 1931)
monoecious, the latter with diverse distributional

patterns of staminate and pistillate flowers
(Kirkup et al. 2000). Inflorescence a sessile or
peduncled, determinate, flabellate dichasium
(sometimes 5-flowered), solitary or fascicled,
axillary and/or terminal; in monoecious species,
central (or only) flower usually staminate, lateral
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Javanese Loranthaceae and the role birds play in 7–9.
their life-history. Beaufortia, Miscell. Publ. 4: Kuijt, J. Dong, W.-X. 1989. Some ultrastructural aspects of
104–207. phloem in Phacellaria (Santalaceae) and Korthalsella
Engler, A., Krause, K. 1908. Uber die Lebensweise von (Viscaceae). Acta Bot. Neerl. 38: 287–293.
Viscum minimum Harvey. Ber. Deutsch. Bot. Ges. Kuijt, J., Wiens, D., Coxson, D. 1979. A new androecial
26a: 524–530. type in African Viscum. Acta Bot. Néerl. 28:
Ernst, E., Schmidt, K., Steuer-Vogt, M.K. 2003. Mistletoe 349–355.
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cal trials. Int. J. Cancer 107: 262–267. mistletoe Arceuthobium douglasii (Viscaceae) in
Feuer, S., Kuijt, J. 1982. Fine structure of mistletoe pollen. host apical buds. Ann. Bot. 97: 953–963.
IV. Eurasian and Australian Viscum L. (Viscaceae). Nickrent, D.L., Garcı́a, M.A., Martı́n, M.P., Mathiasen, R.
Amer. J. Bot. 69: 1–12. L. 2004. A phylogeny of all species of Arceuthobium
Gedalovich, E., Kuijt, J., Carpita, N. 1988. Chemical (Viscaceae) using nuclear and chloroplast DNA
composition of viscin, an adhesive involved in sequences. Amer. J. Bot. 9: 125–138.
dispersal of the parasite Phoradendron californi- Nickrent, D.L. et al. 2010. A revised classification of San-
cum (Viscaceae). Physiol. Mol. Plant Pathol. 32: talales. Taxon 59: 538–558.
61–76. Olson, A.R., Kuijt, J. 1985. Sieve elements in the morpho-
Gómez-Sánchez, M., Sánchez-Fuentes, L.J., Salazar-Olivo, logically reduced mistletoe, Viscum minimum Har-
L.A. 2011. Anatomı́a de especies mexicanas de los vey (Viscaceae). Amer. J. Bot. 72: 1220–1224.
géneros Phoradendron y Psittacanthus, endémicos Olson, A.R., Kuijt, J. 1986. Early development of the pri-
del Nuevo Mundo. Rev. Mex. de Biodiversidad 82: mary haustorium of Viscum minimum (Viscaceae).
1203–1208. Can. J. Bot. 64: 1075–1080.
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Player, G. 1979. Pollination and wind dispersal of pollen Thoday, D. 1958. Id., III. Further observations on Viscum
in Arceuthobium. Ecol. Monogr. 49: 73–87. and Korthalsella. Proc. Royal Soc. B, 148: 188–206.
Restrepo, C. 1987. Aspectos ecologicos de la diseminación Thoday, D. 1961. VI. A general survey of the Loranthoi-
de cinco especies de muérdagos por aves. Humbold- deae. Proc. Royal Soc. B, 155: 1–25.
tia 1: 65–116. Tubeuf, K. von 1923. Monographie der Mistel. Munich
Rizzini, C.T. 1950. Sôbre “Phoradendron fragile” Urb. and Berlin: Oldenbourg.
Rev. Brasil. Biol. 10: 45–58. Watson, D.M. 2011. Mistletoes of Southern Australia.
Rzedowski, J., Calderón de R., G. 2011. Dos especies Collingwood, Australia: CSIRO Publishing.
notables de Phoradendron (Viscaceae) de la Mixteca Wiens, D., Barlow, B.A. 1975. Permanent translocation
(México), una nueva y una complementada. Acta heterozygosity and sex determination in East African
Bot. Mex. 96: 3–10. mistletoes. Science 187: 1208–1209.
Schaeppi, H., Steindl, F. 1945. Bl€utenmorphologische und Wiens, D., Barlow, B.A. 1979. Translocation heterozygos-
embryologische Untersuchungen an einigen Vis- ity and the origin of dioecy in Viscum. Heredity 42:
coideen. Vierteljahrsschr. Naturforsch. Gesellsch. 201–222.
Z€urich 90: 34–46. Wiens, D., DeDecker, M. 1972. Rare natural hybridization
Scharpf, R.F., Hawksworth, F.G. 1976. Luther Burbank in Phoradendron (Viscaceae). Madroño 21: 395–402.
introduced European mistletoe into California. Pl. Wilson, C.A., Calvin, C.L. 1996. Anatomy of the dwarf
Disease Reporter 60: 739–742. mistletoe shoot system. In: Hawksworth, F.G.,
Schmid, R., Calvin, C.L., Wilson, C.A. 2011. Sinker struc- Wiens, D., Dwarf mistletoes: biology, pathology,
ture of Phoradendron californicum (Viscaceae) con- and systematics. U.S.D.A., For. Serv., Agric. Handb.
founds its presumed close relationship to other 709: 95–111.
acataphyllous species. Aliso 29: 13–23. York, H.H. 1913. The origin and development of the
Steindl, F. 1935. Pollen- und Embryosackentwicklung bei embryo sac and embryo of Dendrophthora opun-
Viscum album L. und Viscum articulatum Burm. Ber. tioides and D. gracilis. I and II. Bot. Gaz. 56:
Schweiz. Bot. Gesellsch. 44: 343–388, Taf. 17–23. 89–111, 200–216.
Tainter, E.H. 1968. The embryology of Arceuthobium Zaki, M., Kuijt, J. 1994. Ultrastructural studies on the
pusillum. Can. J. Bot. 46: 1473–1476. embryo sac of Viscum minimum. II. Megagameto-
Thoday, D. 1951. The haustorial system of Viscum album. genesis. Can. J. Bot. 72: 1613–1628.
J. Exper. Bot. 2: 1–19. Zaki, M., Kuijt, J. 1995. Ultrastructural studies on the
Thoday, D. 1956a. Modes of union and interaction embryo sac of Viscum minimum. I. Megasporogene-
between parasite and host in the Loranthaceae. I. sis. Protoplasma 185: 93–105.
Viscoideae, not including Phoradendreae. Proc. Zonneveld, B.J.M. 2010. New record holders for maxi-
Royal Soc. B, 145: 531–548. mum genome size in eudicots and monocots. J.
Thoday, D. 1956b. Id., II. Phoradendreae. Proc. Roy. Soc. Bot., Article ID 527357, doi: 10.1155/2010/527357,
B, 146: 320–338. 4 pp.
Ximeniaceae
Ximeniaceae Horan., Prim. Lin. Syst. Nat.: 72 (1834).
Olacaceae subfam. Dysolacoideae Engler tribe Ximenieae Engler (1897).
Tall or moderately tall trees or shrubs, at least KEY TO THE GENERA OF XIMENIACEAE
Ximenia parasitic on roots of other plants. Leaves
alternate, simple, estipulate, petiolate, venation 1. Umbels subtended by a whorl of small, round-tipped
pinnate or (Curupira) palmate. Inflorescence an bracts; Brazil
axillary umbel (sometimes flowers solitary in 2
Ximenia). Flowers bisexual; calyx 4–5-lobed, not – Umbels not subtended by bracts; paleotropics and
neotropics, NE Australia and China
accrescent in fruit; petals 4 (mostly 8 in Ximenia),
3
adaxially hairy at least in part; stamens mostly 2. Venation palmate, with two basal veins reaching the
twice as many as petals when the latter fewer than apex; floral pedicels slender; petals hairy along mar-
8, rarely 3 x as many (Curupira), both opposite gins; stamens exserted, 1 cm long
petals and alternate with them, distinct; ovary 1. Curupira
elongate, 2–4-loculate; ovules linear, pendent – Venation pinnate; floral pedicels stout; petals hairy
from a central columella. Fruit a 1-seeded below the middle; stamens included, 5 mm long
drupe; embryo dicotylous. 2. Douradoa
Ximeniaceae form a small family character- 3. Ramal, axillary thorns frequent; leaves with terminal
ized by bisexual flowers, a calyx of 4 or 5 mem- prickle; petals densely bearded adaxially; ovary 4-locular;
bers not accrescent in fruit, 4 or 8 petals that are pantropical and some subtropical areas, NE Australia
4. Ximenia
hairy adaxially or marginally, distinct stamens
– Ramal thorns absent; leaf apex without prickle; petals
often twice as many as the petals and both oppo- lanate below the middle; ovary 2-locular below, becom-
site them and alternating with them and bearing ing 1-locular above; China
linear anthers, and a superior ovary with pen- 3. Malania
dent, strikingly linear ovules.
Fossil pollen of Ximenia has been recorded
from the Lower Pleistocene of Olduvai, Tanzania, GENERA OF XIMENIACEAE
a region within its present distributional range
(Bonneville et al. 1982). This study also presents a 1. Curupira G.A. Black Fig. 70
brief characterization and excellent illustrations
of extant Ximenia pollen: tectum smooth to Curupira G.A. Black, Bol. Técn. Inst. Agron. Norte 15:
perforated or reticulate, endoaperture large, 1–32 (1948); Sleumer, Fl. Neotrop. 38: 131–132, Fig. 16
square to rectangular. (1984).
Four genera are currently recognized, in trop-
ical as well as subtropical (Malania, Ximenia) Trees to 25 m high. Leaves alternate, petiolate,
regions of the World. ovate, gradually acuminate, glabrous, with 2 basal
188 Ximeniaceae
Fig. 70. Ximeniaceae. Curupira tefeensis. A Flowering

branch. B Inflorescence. C Flower. D Petal. E Calyx and
ovary. F Anther. G Drupe. (Sleumer 1984)
lateral veins running into the leaf apex. Inflores-

cence a slenderly pedunculate, axillary umbel
with 10–12 flowers subtended by an involucre of
thick, glandular, bract-like structures. Flowers
bisexual, on slender pedicels 1–2 cm long; calyx
cupular, obtusely 4–5-dentate; petals 4, linear-
oblong, hairy along their margins; stamens
8 (sometimes 12), exserted for ca. 1 cm at anthe-
sis, very delicate; anther minute, terminal, fusi-
form; ovary subcylindrical, tapering apically to a
Fig. 71. Ximeniaceae. Douradoa consimilis. A Flowering
small stigma, longitudinally grooved. Fruit an twig. B Inflorescence, partly deflowered. C Flower. D Petal
obpyriform drupe, pericarp thin. from inside. E Pedicel and ovary. F Branchlet with sub-
One rare sp., Curupira tefeensis G.A. Black, mature fruit. (Sleumer 1984)
Brazil: Amazonas, Tefé. Closely related to Dour-
adoa (see for additional comments). The fatty
substances of the fruit are locally used to make hairy below the middle; stamens (7) 8, distinct,
soap. opposite and alternating with and shorter than
2. Douradoa Sleumer Fig. 71 the petals; filaments short and slender; anthers
basifixed, dehiscing longitudinally; ovary superior,
Douradoa Sleumer, Fl. Neotrop. 38: 136–138, Fig. 19 distinct, style short, with minute, sessile stigma.
(1984). Fruit a drupe, erect on an enlarged pedicel, sub-
globose to ellipsoid, with a single seed; pericarp
Large trees. Leaves alternate, petiolate, pinnately coriaceous; endosperm copious, oily.
veined, with distinctive marginal areoles; resin One sp., Douradoa consimilis Sleumer; Brazil:
tubes or laticifers absent. Inflorescence an axillary, Amapá.
pedunculate umbel of 8–10 flowers subtended by The genus is close to Curupira and could
an involucre of small, rounded-tipped bracts. perhaps be united with it, differing in its striking
Flowers bisexual, on stout pedicels, 4-merous; leaf venation, the stout pedicel, included stamens,
calyx of 4 minute lobes; petals distinct, densely a much reduced calyx, and foliar anatomy.
References 189
these sometimes on short-shoots, glabrous,

with rounded tips bearing a minute needle,
with axillary ramal thorns. Inflorescence an
axillary pedunculate umbel of 2–4 flowers or
flowers solitary. Flowers fragrant, usually
bisexual, with 4- or 5-parted, non-accrescent
calyculus; petals usually 8, rarely 4, 5, or 10,
often recurved in anthesis, densely covered
adaxially with reddish-brown to white hairs;
stamens 8–10, half of them opposite, and half
of them alternate with the petals, some epipe-
talous and even with sessile anthers, others
with thread-like, distinct filaments, anthers lin-
ear to globose, basifixed; ovary narrowly coni-
cal, tapering into a long, slender style with
small, capitate stigma; ovarian cavities 4, each
with a single, unitegmic ovule pendent from
the top of a central column. Fruit an ovoid to
spherical, plum-like drupe, yellow to orange,
rarely scarlet; pericarp thin, pulpy, endocarp
hard, below which is an air-bearing tissue;
Fig. 72. Ximeniaceae. Ximenia americana var. ameri- one seed per fruit; germination cryptocotylar.
cana. A Flowering branchlet. B Flower bud. C Flower n ¼ 12, 24, or 13, 26.
with two petals removed. D Drupe. (Sleumer 1984)
At least 10 closely related spp., tropical and
subtropical New and Old World, including one
3. Malania Chun & S.K. Lee sp. in NE Australia.
Ximenia is cryptocotylar in its germination
Malania Chun & S.K. Lee, Bull. Bot. Lab. N.-E. Forest. (Kuijt 1969, his Fig. 3-24d; see also the illustration
Inst. 1980 (6): 67–72 (1980). in Musselman and Mann 1977). Its germination is
peculiar in that the two lowest phyllomes bend
Trees; leaves alternate, subcoriaceous. Flowers back to insert themselves into the space between
small, inflorescence an umbel, pedicels filiform; the two cotyledons.
calyx small, 4-lobed; petals 4, valvate, lower In Namibia, a minor industry is based on oils
inside lanate; stamens twice as many as petals; expressed from two native Ximenia species. The
filaments filiform; anthers linear, erect, bilocular, fleshy part of the fruit is edible. The genus is also
basi-/dorsifixed, longitudinally dehiscent; ovary important in local medicine in Rio Grande do
superior, 2-loculed below, 1-loculed above, Norte, Brazil.
stigma minutely 2-lobed; ovules 2, linear, pen-
dent from the tip of the placenta. Drupe subglo-
bose, its base slightly contracted. Seed globose, References
with copious, fleshy endosperm. n ¼ 13.
One sp., Malania oleifera Chun & S.K. Lee,
endemic to China. de Ximenia (Olacaeae) dans le Pléistocène Inférieur
d’Oldouvai en Tanzanie: implications paléoécologi-
4. Ximenia L. Fig. 72 ques. J. Biogeogr. 9: 469–486.
Kuijt, J. 1969. The biology of parasitic flowering plants.
Ximenia L., Sp. Pl.: 1193 (1753); Sleumer, Fl. Neotrop. 38: Berkeley and Los Angeles: Univ. Calif. Press.
88–99 (1984). Musselman, L.J., Mann, W.F. 1977. Cataphyll behavior in
Ximenia americana seedlings (Olacaceae). Beitr.
Biol. Pflanzen 53: 121–125.
Semiparasitic, low trees or shrubs with ovate- Sleumer, H. 1984. Olacaceae. Flora Neotropica 38: 1–159.
lanceolate, alternate, pinnately veined leaves, New York: Organiz. For Fl. Neotrop.
BALANOPHORALES
By B. Hansen (deceased)1
Only one family.
1
This contribution is based on a manuscript that Bertel Hansen (deceased 2004) prepared around 1978, on request of the late
Rolf Dahlgren, in the early time of the initiation of this book series as a model treatment. During the last decades, our
knowledge of the family has greatly expanded not least due to later work by Dr. Hansen. His publications have been of great
utility for me when preparing this updated version, with which Dr. Hansen leaves his imprint on this book series.
K. Kubitzki
Balanophoraceae
Balanophoraceae L.C. Richard, Mém. Mus. Hist. Nat. Paris 8: 429 (1822), nom. cons., “Balanophoreae”.
Herbaceous, fleshy root parasites devoid of 1-locular or without a cavity or any definite pla-
chlorophyll and normal roots, developing at the centa; stigmas inconspicuous or slightly capitel-
point of contact with a host root a subspherical late. Generally one few-celled embryo developing
or irregularly lobed or branched subterranean in the central tissues of the ovary, surrounded by
corrugated or warty tuber sometimes provided a few-celled endosperm and a layer of stone cells
with stolon-like “runners”; the tubers containing at maturity. Fruit a very small, 1-seeded drupe
starch or less often a wax-like substance; inflor- enclosed in an initially fleshy and later mostly dry
escences mostly supraterranean, arising either exocarp and a sclerotised endocarp; embryo very
directly from the tuber or from a runner, their small; endosperm well developed.
peduncles unbranched, bearing leaves or leafless; A mainly tropical or subtropical family with
the leaves scaly, usually spiral, rarely opposite, 42 species in 16 genera.
decussate or distichous, rarely verticillate, some-
times much reduced or lacking completely (Bala- MORPHOLOGY AND ANATOMY. The vegetative bodies
nophora), devoid of stomata; the terminal spadix or “tubers” of the Balanophoraceae develop on
branched or unbranched, branches of first order host roots and remain permanently in contact
bracteate, well-developed to totally suppressed; with them for the uptake of water and nutrients.
bracts scaly, caducous or persistent, triangular They range from tiny (>1 mm) when first appear-
or reduced, clavate, sometimes with the sterile ing on the host root to several decimetres in
apical part peltately widened. Flowers unisexual, diameter and may be spherical, lobed, sometimes
plants monoecious or dioecious; staminate flow- (as in Langsdorffia) ramified and may produce
ers with 2(3), less often 4–8 basally connate or horizontal, stolon-like, relatively thin (up to
distinct valvate perianth segments; stamens 3–4 8 mm thick) “runners” which can contact with
or 1–2, opposite the perianth segments, the nearby host roots. The tubers lack a typical stem
anthers distinct and dehiscing longitudinally or or root organisation, including all vegetative
connate into a synandrium; pistillate flowers usu- organs found in green land plants such as
ally perianthless, rarely with a 3-lobed (Mystro- roots,1 leaves, and axillary buds and usually also
petalon) or an inconspicuously 2-lobed perianth; an epidermis; in some Balanophora they are
gynoecium with distinct stylodia alternating covered by two types of cells which at maturity
with the perianth lobes, or the stylodia connate are empty and thick-walled and clump together in
into a single style; carpels not recognizable; ovary irregular masses (“armature cells”) or form 4- or
1
The vegetative body of Thonningia consists of long, branching, horizontal cylinders, which Mangenot (1947) interpreted as
roots provided with root caps, although this may be due to an error because, as Mauseth et al. (1992) commented, the line
drawings accompanying Mangenot’s paper refer to a structure quite different in diameter from the massive elongate tuber. In
Corynaea crassa short, numerous, about 4 mm long unbranched structures without a true epidermis were observed to develop
from the surface of the tuber (Kuijt and Bruns 1987). These are the only indications for a possible occurrence of roots in
Balanophoraceae known to me certainly worth of re-investigation.
194 Balanophoraceae
5-radiated clusters of cells, the “stellate warts” Although there is much variation in the shap-
(Kuijt and Dong 1990a), whereas a more regular, ing of the host/parasite interface, two basic types
epidermis-like pattern occurs only occasionally can be recognized. In Helosis and Ombrophytum
(in Langsdorffia hypogaea, Hsiao et al. 1994) the interface is a rather simple fluted disk in
and is often interrupted by warts made up largely which a discrete host surface meets a discrete
of brachysclereids. Hairs are rarely found in veg- parasite surface, where vessel contact between
etative parts but have been observed as a dense the two partners is achieved. No host tissue is
cover of unicellular trichomes on the tubers of present in the parasite portion of the tuber (Mau-
Langsdorffia. The tubers grow by the prolifera- seth et al. 1992; Hsiao et al. 1993), and the vascu-
tion of parenchyma cells and are penetrated by lar supply of the tuber including central and
a network of vascular bundles usually produced collateral bundles exclusively belongs to the par-
by the parasite, which are capable of secondary asite. In Balanophora (Fagerlind 1948; Gedalo-
growth. The runner primordia are initiated in vich-Shedletzky and Kuijt 1990; Hsiao et al.
tubers or on older runners; they were found 1995) and Langsdorffia (Hsiao et al. 1994) the
both in Helosis and Ombrophytum to possess tuber contains two vascular systems, one pro-
an epidermis and an apical meristem with a duced only by the parasite, and another one
tunica/corpus zonation and a vascular tissue consisting of “composite bundles” which contain
with eustelic organisation but to lack a root cap vascular tissue of both the host and the parasite.
and endodermis (Mauseth et al. 1992; Hsiao et al. Obviously, the host is induced by the parasite to
1993). In addition to the bundles produced by the produce procambial strands into the proliferating
parasite, the tubers of Thonningia, Langsdorffia tuber tissue, which may be interpreted as mod-
and Balanophora contain bundles comprising tis- ified lateral roots of the host growing intrusively
sue from the host and the parasite, which grow by through the parasite tissues of the tuber (Hsiao
virtue of an chimaeral apical meristem (see et al. 1994). Tracheary elements begin to differ-
below). entiate in these procambium strands, which will
be surrounded by a sheath of parenchyma con-
GERMINATION, INFECTION, AND THE HOST/PARASITE sisting of parasite cells. Within this sheath, a
INTERFACE. In Balanophora the seeds germinate cambium is formed which produces xylem and
only close to a host rootlet (Fagerlind 1948), and phloem and connects with the cambium of the
the endosperm cells closest to the rupture elon- host. The central conducting tissue of these bun-
gate and send out 4–8 narrow, tubular and appar- dles will be invaded by large parasite transfer
ently sticky extensions which anchor the fruit to cells, which will connect with the tracheary ele-
the rootlet [see also the photograph of the actual ments of the host and eventually will take part in
invasion of host tissues in the germination of a closely integrated chimeric apical meristem. In
Balanophora elongata by Weber and Sunaryo this sophisticated form of host/parasite interface,
1990]. The few-celled embryo sends out 1–4 direct contact between the two partners occurs
thick tubular processes containing dense cyto- exclusively by means of the parasite transfer cells
plasma and comparatively large nuclei, the pri- in the composite bundles.
mary haustoria. Simultaneously the upper A peculiar host/parasite interface of complex-
embryo cells through a series of divisions pro- ity intermediate between the two types described
duce a whitish nodule of parasite parenchyma above is known from Dactylanthus (Moore 1940)
(Govindappa and Shivamurthy 1976). The and Lophophytum (Gonzalez and Mauseth 2010),
entrance of the haustoria into the host rootlet where the attachment with the host is a discrete
induces the root tissue of the host to proliferate woodrose caused by the proliferation of host
and grow into the tuber. When the tip of the wood on a “coralloid” interface.
radicle of the seedling touches a host root it
forms a spherical haustorial structure; in Dacty- VEGETATIVE REPRODUCTION. Several members of the
lophora root hairs of the radicle are orientated Balanophoraceae are capable of reproducing by
towards the host root surface and become firmly runners produced by the tuber which establish
attached to it, thus securing the rootlet to the host new plants at some distance from the mother
root (Moore 1940; Holzapfel 2001). plant. In Helosis (Hsiao et al. 1993) and
Balanophoraceae 195
Ombrophytum (Mauseth et al. 1992), elongate doideae, the young inflorescences are covered by
runners differing significantly from the structure the marginally coherent peltas of peltate scales.
of the main tuber form haustoria which can infest These have been interpreted by Fagerlind (1945a)
new host roots, whereas in Thonningia and as the sterile, peltately widened apical parts of
Langsdorffia the contact is achieved by any por- secondary axes. In this respect, the Helosidoideae
tion of the hairy tuber (Mangenot 1947; Hsiao agree with some Lophophytoideae. In Lophophy-
et al. 1994). In Dactylanthus taylorii, root-like tum, the peltas of the peltate bracts are angularly
structures surrounding the sheath of the inflores- ovate and have a sickle-shaped pouch into which
cence peduncles even at a time when these have the lower parts of the nearest three distal peltas
not yet broken through the cortex of the tuber are inserted (Fig. 73). The spadices of some
were discovered by Moore (1940) and further Ombrophytum and Latrophytum have bracts
studied by Holzapfel (2001); they exhibit great with imbricate, hexagonal peltas and, in Scyba-
similarity with the radicle of germinating seeds lium, some species have epeltate scales with a
and, like these, attach to and infest host roots by transversely extended petiole along the lower
means of their terminal portion. As long as the margin, where the flowers are inserted. In Bala-
connection between the source plant and its veg- nophora, the pistillate flowers are densely covered
etatively produced tubers remains intact, a large by peculiar, club-shaped organs, the so-called
complicated network of flowering tubers may spadicles, which have been interpreted as mod-
result which represents a single individual. On ified phyllaries or widened, sterile parts of inflo-
the other hand, large, lobed tubers of the dioe- rescence branches; the pistillate flowers are
cious Dactylanthus have been found to be com- inserted among them or on the lower part of the
posed of individuals of different sex which are the spadicles. The staminate inflorescences of Bala-
result of different infections, as has been con- nophora have inconspicuous bracts which may be
firmed by genetic markers (Holzapfel 2001). much reduced. For further details see Hansen and
Engell (1978) and Eberwein et al. (2009).
INFLORESCENCES. The aerial shoots of the Balano-
phoraceae break through the coriaceous cover of FLOWER STRUCTURE. The flowers of Balanophora-
the tuber, often leaving a basal sheath, the ceae are unisexual and obviously have undergone
“volva”. The inflorescence peduncles often bear a wide range of reductions; they are either dioe-
scaly leaves in spiral phyllotaxis; they and virtu- ciously or monoeciously distributed. In the sta-
ally the whole plant are devoid of stomata (Kuijt minate flowers, 4–6 perianth segments are found
and Dong 1990b). Three vascular bundles are in most Balanophora spp., whereas in one subge-
found basally in the leaves of Langsdorffia hypo- nus of Balanophora as well as in all Scybalioideae,
gaea and Lophophytum mirabile and one bundle in Mystropetalon and in Hachettea the perianths
in Scybalium fungiforme. In Scybalioideae and are trimerous. Dactylanthus has two much
Helosidoideae the flowers are embedded in a reduced perianth segments and in Lophophytoi-
dense layer of filiform, multicellular hairs, which deae the two segments hardly can be recognized.
in Rhopalocnemis excrete a sugary liquid. The In Lathrophytum there is no trace at all of peri-
inflorescence-bearing peduncles in Helosis con- anth segments. The stamens are quite normal
tain 12–20 vascular bundles in two basal rings; (tetrasporangiate) and distinct in Mystropetalon,
their number increases above by ramification, as well as Dactylanthoideae and Lophophytoi-
and profuse branching occurs in the spadix. deae. In Sarcophytoideae the anthers are multi-
The inflorescences of Sarcophyte and Chla- locular and, in Helosidoideae, Scybalioideae and
mydophytum are twice branched and break in a Balanophoroideae, they are connate into synan-
fully developed stage directly through the cortex dria.
of the tuber, whereas in all other genera the In the pistillate flowers, Hachettea and
inflorescences are once branched and often form Mystropetalon have three epigynous segments,
a distinct spadix. In Hachettea and Dactylanthus connate below into a short tube. Thonningia
the floral parts are covered by the same bracts as and Langsdorffia have epigynous, tubular peri-
are found on the peduncle beneath them. In Helo- anths with small, inconspicuous segments. In
sis, Corynaea and the other genera of the Helosi- Scybalioideae there are two epigynous, lip-like
196 Balanophoraceae
No definite ovarian cavity is found in the

members of this family, nor is a well-defined
placenta seen. Consequently, normal ovules are
not developed, and the ovules may be regarded
ategmic and there exists a close connation
between the nucellus and the ovary wall. The
female gametophyte develops following the
Allium or Polygonum type. Endosperm develop-
ment is cellular ab initio. So far, embryos of
Balanophoraceae have mostly been described as
small and globular and always lacking cotyle-
dons.
In a survey of pollen and stigma conditions
within the family (Hansen 1976a), which covered
the majority of the genera, most genera were
found to have binucleate pollen, whereas the
three-nucleate condition appeared only in the
Helosidoideae. In spite of the excessive reduction
of all reproductive organs in the family, Sato and
Gonzalez (2013) found in two species of Lopho-
phytum a quite normal microspore and microga-
mete development.
Fig. 73. Balanophoraceae. Detail of inflorescence struc-
ture of Lophophytum weddellii. A Single bract in front PALYNOLOGY. (See also the generic descriptions.)
view and the corresponding axillary (in this case pistil- The family as a whole is eurypalynous. Tricolpo-
late) inflorescence branch. B Longitudinal section of A, rate grains occur in Lophophytoideae and tricol-
with the next higher bract shown by dotted lines. (From
Hansen and Engell 1978) pate grains in Helosidoideae. Triporate grains are
found in Balanophoroideae and Sarcophytoideae,
while pantoporate grains occur in Balanophora,
Scybalium and Dactylanthoideae. Inaperturate
structures concealing the basal parts of the stylo- grains have been found in subgenus Balania of
dia and interpreted as perianth segments by Balanophora (Hansen 1980, 1982, 1984, 1986).
various authors. In Lophophytoideae two much
reduced segments are found in one species, while KARYOLOGY. In B. abbreviata, B. elongata and B.
the remaining species apparently lack a perianth. fungosa subsp. indica, n¼ca. 16 or ca. 18 and
In Balanophora the pistillate flower is reduced to 2n¼ca. 36 have been reported. The obviously
a pistil composed of a swollen ovary and a fili- apomictic B. japonica had 2n¼56 or 94–112
form style. In Sarcophyte and Chlamydophytum (Hansen 1972). Earlier reports on B. dioica were
the female flowers are assembled in small, fleshy, due to misidentification. Mangenot (1947) found
globular heads, each flower distinguished only by in Thonningia n¼ca. 18.
its stigma protruding from the surface of the
head. POLLINATION AND DISPERSAL. These topics are little
known for the family, not least because of the
EMBRYOLOGY. Apart from Fagerlind’s (1938, 1945a) often more or less subterranean nature of the
and Umiker’s (1920) investigations, very little is reproductive process: apart from Helosidoideae
known of the embryology of neotropical taxa. and Balanophoroideae, sometimes only the distal
More observations are available for palaeotropi- portion of the spadix with the pistillate flowers
cal taxa. However, much of the information emerges above ground level. Nevertheless, insect
concerning Balanophora is contradictory accord- pollination is highly probable in many species
ing to Fagerlind (1945b), who reviewed earlier of Balanophoraceae; the pollinators are attracted
investigations in detail. by sugary excretions in the inflorescences, as
Balanophoraceae 197
observed in Rhopalocnemis by van Steenis (1932); PHYTOCHEMISTRY. It has long been known that the
Diptera as flower visitors and probable pollina- tubers of Balonophora species contain a waxy
tors were observed on different spp. of Balano- constituent extractable by ether, the “balano-
phora, Lophophytum and Sarcophyte (Knuth phorin” (Goeppert 1841), of which 90% is
1904; Zweifel 1939), small Hymenoptera have b-amyrin-palmitate (Ultée 1926). Balanophorin
been seen to visit Balanophora fungosa subsp. seems to be restricted to Balanophoroideae,
indica (Hansen 1972) and B. abbreviata (Govin- whereas in the tubers of most other subfamilies
dappa and Shivamurthy 1975), and Coleoptera starch is accumulated, often in large quantities.
were attracted by a strong scent emitted by Tannins seem to be generally present, although
Lophophytum mirabile (Borchsenius and Olesen their exact nature remains unknown, and the
1990). Over a time span of two weeks at night and search for other compounds including alkaloids,
day large quantities of nectar are produced in saponins and fatty acetylenic acids was unsuc-
Dactylanthus taylorii by the pistillate individuals; cessful (Hegnauer 1964).
much pollen from nearby staminate plants is
added to it, and pollination is achieved mainly SUBDIVISION AND CIRCUMSCRIPTION OF THE FAMILY.
by the endemic short-tailed bat Mystacina tuber- Griffith (1846) and Hooker f. (1856) divided the
culata accompanied by various insects and mam- family into Monostyli and Distyli, but Eichler
mals such as the common ship-rat (Rattus rattus) (1873) abandoned the number of stylodia as the
and the possum (Ecroyd et al. 1995; Ecroyd 1996). main subdivision criterion. He used a combina-
Pollination of the subterranean flowers of Ombro- tion of several characters for his eight tribes,
phytum is still unknown. which were largely identical with groups already
In many species the formation of pollen tubes defined and named by Hooker f. but without
penetrating the stylar tissues has been observed taxonomic status. Engler (1889) erected six sub-
and, in Balanophora abbreviata, Zweifel (1939) families, two of them each combining two of
found cases of double fertilization. Fagerlind Eichler’s tribes, the rest of them identical with
(1938) demonstrated a quite normal process of the remaining tribes. van Tieghem (1907) went
fertilization in Helosis, contrary to the statements very far in splitting the Balanophoraceae into six
by Umiker (1920) regarding this aspect. Apo- families, whereas Harms (1935) divided the
mixis has been proved only in a few Balanophora family into six subfamilies and excluded Cyno-
(Fagerlind 1945b) and is highly probable in morium. Harms also erected a new subfamily,
Ombrophytum subterraneum, especially in popu- Lophophytoideae, but more recently a close re1a-
lations destitute of pollen or with abnormal tionship between Scybalium and the Lophophy-
pollen grains. The fruit is generally a very small, toideae was also revealed with respect to the
1-seeded drupe enclosed in an initially fleshy and morphology of their inflorescences and particu-
later mostly dry exocarp and a sclerotised endo- larly the bracts subtending the inflorescence
carp which encloses the pyrene; the embryo is branches (Hansen and Engell 1978). Scybalium
very small and usually appears spheroid; it lacks of the Scybalioideae is closely linked to Helosi-
cotyledons; endosperm is well developed. doideae through Scybalium depressum in the
Little is known of the dispersal of the propa- development of the subtending bracts as well as
gules. Ant dispersal occurs in Mystropetalum. In in the arrangement of the pistillate flowers. Helo-
Balanophora the fruits are about the same size sidoideae present an extremely uniform develop-
and weight as orchid seeds, and possibly wind- ment throughout their wide geographical range.
dispersed. Their rough fruit wall would make Based on inflorescence characters, particularly
them easily attachable to the bodies of visiting the arrangement of flowers and subtending
insects, but this remains to be observed in the bracts, some affinity between Scybalioideae and
field. Also rain wash must be considered. In South Balanophoroideae may be inferred (Hansen and
American taxa the fruits are much bigger, and Engell 1978). Within Balanophoroideae strong
wind dispersal is unlikely. However, high con- affinities are obvious between Balanophora and
tents of starch in the tissues of most species may Langsdorffia due to striking similarities in the
attract herbivores, which may function as dis- development of the embryo sac (Fagerlind
persal agents. 1945a) as well as in the pollen morphology.
198 Balanophoraceae
More recently, the division of Balanophora- ing from tropical Africa via Madagascar to tropi-
ceae into the six subfamilies by Harms (1935) cal Asia, Malesia, Australia and the Pacific
has been widely accepted—although Takhtajan islands. Langsdorffia has five spp., two in tropical
(1997) returned to treat them as eight distinct America, one in Madagascar and two in New
families; in his last work (Takhtajan 2009) he Guinea. Six genera are restricted to tropical
downgraded these to subfamilies. Until quite America, five to Africa and Madagascar, two to
recently, Cynomorium sometimes has been trea- tropical Asia, one to New Caledonia and one to
ted as a member of Balanophoraceae, which in the North Island of New Zealand.
view of the significant differences between them
(as listed by Takhtajan 2009) virtually is untena-
KEY TO THE GENERA OF BALANOPHORACEAE
ble. Engler’s placement of Cynomorium in
Myrtales (in Engler and Gilg 1924, p. 308) hardly 1. Pistillate flowers inserted on an articulate pedicel later
ever has been taken seriously, but the molecular to become a cushion-like elaiosome; pollen grains (3)4
data available yield discordant results for their (5)-angular and (9–)12(15)-colpate, detaching (at
placement either in the Saxifragales (Nickrent acetolysis) into triangular, tetrangular or pentangular
et al. 2005) or Rosales (Zhang et al. 2009). platelets 1. Mystropetalon
– Pistillate flowers lacking basal articulation; pollen
AFFINITIES. The members of this family were con- grains not detaching into angular platelets 2
sidered as fungi by early authors and later on 2. Inflorescence conspicuously branched, branches of
were placed between the Ferns and the Monoco- first order slender, 2–7 cm long, style single or 0 3
tyledons or between these and the Dicotyledons. – Inflorescence apparently not branched or once
branched, then stylodia 2 and branches of first order
Hooker f. (1856) recognized them as angiosperms
at most 2 cm long 6
and pointed to their flower-morphological simi- 3. Style present, elongated; pistillate flowers singly on
larities with Gunneraceae–Haloragaceae, a posi- thin, elongated branches of first order 4
tion lately retained by Dahlgren (1975), although – Style absent, stigma sessile; pistillate flowers confluent
a position close to Santalales had been advocated into small, fleshy heads on short inflorescence
strongly by most authors in the intermittent branches of 2nd order 5
period. Harms (1935) preferred the placement of 4. Staminate flowers with a conspicuous, 3-lobed peri-
Balanophoraceae in an order separate from San- anth; inflorescence branches of first order inserted on
tales because, in view of the strong structural elongated upper part of stem, subtended by bracts
reduction of the former, he missed a clear mor- 2. Hachettea
phological link between the two; also, Kuijt (1969) – Staminate flowers without a perianth or with two fili-
form perianth lobes; inflorescence branches of first
remained reluctant about their inclusion into
order inserted on slightly swollen apical part of stem,
Santalales. Molecular analyses of the holoparasi- not subtended by bracts 3. Dactylanthus
tic Balanophoraceae employing nuclear 18S 5. Inflorescence bracteate; stamens 3(4), with conspicu-
rDNA and mitochondrial matR regions (Nickrent ous filament; pistillate flowers with conspicuous, disci-
et al. 2005; Barkman et al. 2007) have supported form stigma 4. Sarcophyte
their closeness to Santalales; Su and Hu (2008, – Inflorescence apparently ebracteate or sometimes in
2012), based mostly on B-class homoeotic genes, staminate inflorescences with a minute bract support-
confirmed this finding, even though their exact ing branches of first order; stamens 6–7, without fila-
relationships remained problematic due to the ment; pistillate flowers presenting only the tripartite,
low support for some nodes. Therefore, Balano- sessile stigma 5. Chlamydophytum
phoraceae are treated here as the sole member of 6. Stylodia 2; starch in tubers and elsewhere 7
– Style single; wax in tubers and elsewhere 14
a distinct order, Balanophorales, which does not
7. Flowers embedded in a layer of filiform hairs 8
preclude possible affinities with Santalales. – Flowers not embedded in hairs, on conspicuous,
elongated inflorescence branches of first order sub-
PHYTOGEOGRAPHY. The family is pantropical with tended by often early caducous peltate bracts 12
outliers in the subtropics and adjacent temperate 8. Young inflorescences covered by more or less triangu-
mountain areas. The largest genus, Balanophora lar scales; peduncles densely covered by same kind of
with 15 spp., has its centre with 10 species around scales; pollen grains pantopororate
the Indo-Chinese Peninsula and one species rang- 10. Scybalium
GENERA OF BALANOPHORACEAE 199
– Young inflorescence covered by hexagonal, peltate, Monoecious reddish to yellowish-white plants up

bracts; peduncles naked or at most with reduced, to 25 cm tall, arising from a subspherical, lobed
inconspicuous, bract-like structures; pollen grains tuber; peduncle imbricately leaved. Inflorescence
3-colpate 9 spicate, the lower part with pistillate flowers, the
9. Inflorescences emerging from elongated, stolon-like
upper staminate. Flowers slightly zygomorphic,
“runners” 6. Helosis
– Inflorescences emerging directly from a compact tuber
subtended by a bract and two prophylls; stami-
10 nate flowers with 3 perianth segments valvately
10. Synandrium with one row of 6 vertical pollen sacs arranged and 2 distinct stamens; anthers dorsi-
7. Corynaea fixed, lengthwise dehiscing; pollen grains (9–)12
– Synandrium >15-locular, the locules in 2–3 layers (15)-colpate and (3)4(5)-angular, detaching (at
11 acetolysis) into triangular, tetrangular or pentan-
11. Synandrium 15–20-locular; plant very dark to almost gular platelets; disk short, lobed, encircling a
black; tuber fairly smooth; hardly any sheath rudimentary pistil; pistillate flowers inserted on
8. Ditepalanthus an articulate pedicel later to become a cushion-
– Synandrium 20–30-locular; plant brownish; tuber like elaiosome; perianth segments 3; staminodes
roughly corrugated; sheath conspicuous
2, ovary inferior, obviously 3-merous; style sin-
9. Rhopalocnemis
12. Branches subtended by bracts with angularly-ovate
gle, basally encircled by crenate disk. Fruit almost
pelta; apical part of pistillate branch not peltately spherical, 3 mm diam., with hard exocarp and
enlarged 11. Lophophytum soft endocarp.
– Branches subtended by bracts with hexagonal or One sp., M. thomii Harv., western Cape
more irregularly shaped pelta; apical part of pistillate region of South Africa. Parasitizing species of
branch peltately enlarged, covering the flowers Leucadendron and Protea. Dispersed by ants.
13 A reddish-brown deposit called mystrin is
13. Staminate flowers solitary, each flower subtended by a observed in the tissue of leaves and the cortex of
peltate bract; anthers sessile 13. Lathrophytum the axis but also of flowers and fruits; it is formed
– Staminate flowers in many-flowered branches, each when the tissue is preserved in formaldehyde-
branch subtended by a peltate or clavate bract; pelta
containing fixatives.
sometimes reduced; anthers with a conspicuous fila-
ment 12. Ombrophytum II. SUBFAM. DACTYLANTHOIDEAE Engl. (1889).
14. Pistillate flowers without perianth, consisting of an
ovoid ovary and a filiform stylodium without any Ovary inferior; stamens 1 or 2, distinct or con-
obvious stigma, inserted between numerous clavate nate; pollen grains pantoporate-annulate; stylo-
subtending bracts 16. Balanophora
dia connate into a single style.
– Pistillate flowers with an inconspicuously 3–4-lobed,
tubular perianth and a stylodium with obvious stig- 2. Hachettea Baillon Fig. 74
matic apical part; clavate subtending bracts absent
15
Hachettea Baillon, Bull. Mens. Soc. Linn. Paris: 229
15. Staminate flowers with (2)3 tepals in one cycle
(1880), Dict. Bot. 3: 2. t. 18 (1887); B. Hansen, Acta
14. Langsdorffia
Phytotax. Geobot. 33: 95–96 (1982).
– Staminate flowers with 2–6 spirally arranged (?) tepals
15. Thonningia
Dioecious yellowish brown to reddish plants
15–30 cm tall arising from a spheroid tuber;
GENERA OF BALANOPHORACEAE basal sheath not obvious; peduncle covered by
spirally arranged scaly leaves which in upper
I. SUBFAM. MYSTROPETALOIDEAE Engl. (1889). third gradually become larger and function as
bracts each subtending one inflorescence branch.
Ovary inferior, adnate to calyx tube, basally Flowers subtended by short, reduced bracts, sta-
encircled by irregularly crenate disk; style single; minate ones pedicellate; tepals 3, elliptic, valvate,
ovules 3, pendulous. stamens 2 with very short filaments, anthers ter-
1. Mystropetalon W.H. Harvey minal, dehiscing by transverse slits; pollen grains
asymmetric or centrosymmetric, (3)4(6)-porate-
Mystropetalon W.H. Harvey, Gen. S. Afr. Pl.: 418 (1838); annulate; pistillate flowers sessile, perianth very
B. Hansen, Bot. Jahrb. 106: 370–374 (1986). small, superior, short tubular 3-lobed; ovary
200 Balanophoraceae
Fig. 75. Balanophoraceae. Dactylanthus taylorii. A Habit.

B Part of staminate inflorescence branch. C Staminate
flower. D Pistillate inflorescence branch. E Pistillate
flower. (From Hansen 1982, redrawn after Cheeseman
Fig. 74. Balanophoraceae. Hachettea austrocaledonica. A
1914 by Victoria C.G. Friis)
Habit, staminate plant. B Longitudinal section of pistillate
plant. C Staminate inflorescence branch. D Staminate
flower. E Pistillate inflorescence branch. F Pistillate
flower. (From Hansen 1982, redrawn after Baillon 1891
by Victoria C.G. Friis) at a time from large tubers, with spirally arranged
imbricate scaly leaves which increase in size dis-
inferior, narrowly ovoid, apparently 3-celled; style tally in the inflorescence and form an involucre
single. around the flower-bearing branches, these 15–25,
One sp., H. austrocaledonica Baill., endemic ebracteate, inserted at swollen apical part of ped-
to New Caledonia, in mountain forests, 300–1,500 uncle, each with up to 50 staminate or 100 pistil-
m alt. Parasitizing Cunoniac. late flowers. Staminate flowers usually ebracteate,
sessile; tepals usually 2, lateral; stamen single with
3. Dactylanthus Hook.f. Fig. 75 short and thick filament; anther deeply lobed,
4-locular, dehiscing irregularly; pollen grains
Dactylanthus Hook.f., Trans. Linn. Soc. London 22: 425, asymmetric or centrosymmetric, (3–)10–11-
t. 75 (1859); B. Hansen, Acta Phytotax. Geobot. 33: 96–98 porate-annulate; pistillate flowers sessile; tepals
(1982); Holzapfel, Englera 22: 1–176 (2001). two, minute, linear; ovary inferior, apparently
2-celled; style single.
Dioecious brownish plants 5–15 cm tall, arising One sp., D. taylorii Hook.f., endemic to the
from a large, irregularly lobed tuber; basal sheath North Island, New Zealand. Parasitizing Araliac.,
not obvious. Flowering shoots often more than 20 Cornac., Fagac., Loganiac., Monimiac., Myrsinac.,
Pittosp., Rubiac. The plant appears to be dioe-

cious; if plants of both sexes appear from a lobed
tuber, this may be a chimera.
III. SUBFAM. SARCOPHYTOIDEAE Engl. (1889).
Inflorescence conspicuously branched, panicu-

late; pollen grains 3-porate; stigma sessile.
4. Sarcophyte Sparrman Fig. 76
Sarcophyte Sparrman, Kongl. Vetensk. Acad. Handl. 37:

300, t. 7 (1776); B. Hansen, Bot. Jahrb. 106: 364–366
(1986).
Dioecious, red to dark red, conspicuously

branched plants up to 20 cm tall, arising from
large, polygonately furrowed tubers; above-
ground parts breaking through the surface of
the tuber which leaves a short, irregularly lobed
sheath around the base of the peduncle; peduncle
bracteate, bracts spiral; spadix paniculate; stami-
nate flowers many on secondary branches, 3(4)-
merous, tepals valvate, stamens with thick fila- Fig. 76. Balanophoraceae. Sarcophyte sanguinea. A
ments and globular multilocular anthers; pollen Habit. B One branch of staminate inflorescence. C Stami-
nate flower. D A tepal with a sectioned anther. E Longitu-
grains triporate, rugulose; pistillate flowers in dinal section of a capitulum with sunk pistillate flowers.
5–12 subglobular clusters on each branch each (From Harms 1935)
comprising about 200 flowers completely sunk
in the receptacle; stigmas discoid, peltate on a tepals; antetepalous stamens with some additional
very short style, almost covering the surface of ones scattered on the receptacle, the anthers ses-
the receptacle; ovary 3(4)-merous. sile, multilocular; pollen grains suboblate-spher-
One sp. with two subsp., S. sanguinea Sparr- oid, triporate, exine gemmate; pistillate flowers in
man, tropical East Africa and South Africa. 15–20 clusters on each branch and about 100
Parasitizing Burserac., Legum., Meliac., Morac., flowers in each cluster, completely sunk in the
Palmae, Sapotac. receptacle, 3(4)-merous, presenting only the ses-
sile stigmatic lobes; ovary 3(4)-merous.
5. Chlamydophytum Mildbraed One sp., C. aphyllum Mildbraed Cameroons
and Congo, rarely collected. Parasitizing Legum.
Chlamydophytum Mildbraed, Verh. Bot. Vereins Prov.
Brandenburg 67: 196 (1925); N. Hallé, Adansonia II, 17: IV. SUBFAM. HELOSIDOIDEAE Tiegh. (1898).
249, pl. 1–8 (1978); B. Hansen, Bot. Jahrb. 106: 367–368
(1986). Inflorescence when young covered by hexagonal,
peltate bracts, its peduncle without scaly leaves;
Dioecious, dark flesh-coloured plants up to 45 cm flowers immersed in a layer of chaffy hairs; pollen
tall, arising from an irregular cylindrical tuber grains 3-colpate.
covered with polygonal warts; above-ground
parts breaking through the coriaceous surface of 6. Helosis L.C. Richard Fig. 77
the tuber; peduncle ebracteate or minutely brac-
teate; spadix paniculate, branches subtended by Helosis L.C. Richard, Mém. Mus. Hist. Nat. 8: 416, 430,
minute bracts or bracts lacking. Staminate flowers 432, t. 20 (1822), nom. cons.; B. Hansen, Fl. Neotrop. 23:
2(3) together, sessile, with (5)6–8(9) triangular 33–41 (1980).
202 Balanophoraceae
locules; pollen grains suboblate, psilate, tricolpate

(only known in H. cayennensis); pistillate flowers
naked or with 2 perianth segments, stylodia 2,
surmounting the layer of hairs, stigmas capitel-
late. Fruit a small, 1-seeded achene.
Two spp., H. cayennensis (Swartz) Spreng.,
Central and South America from Mexico to SE
Brazil, below 1,500 m. alt., parasitizing Legum.,
Morac., Sapotac., Urticac., and H. ruficeps (Ridl.)
R.K. Eberwein, Malayan Peninsula.
7. Corynaea Hook.f. Fig. 78
Corynaea Hook.f., Trans. Linn. Soc. London 22: 31, 54,

t. 13 (1856); B. Hansen, Fl. Neotrop. 23: 41–45 (1980).
Monoecious yellowish-brown to deep purple or

rarely whitish plants with usually a number of
inflorescences up to 15 cm long arising from a
large irregularly lobed tuber; peduncles leafless.
Inflorescence bisexual, spadiciform, when young
covered by hexagonal, peltate, caducous bracts.
Flowers embedded in a dense layer of filiform
hairs, the staminate ones with a 3-lobed or irre-
gularly crenate perianth; stamens 3, connate,
synandrium with 6 vertical locules; pollen grains
suboblate, psilate, 3-colpate; pistillate flowers
Fig. 77. Balanophoraceae. A Helosis cayennensis subsp. compressed, with 2 inconspicuous perianth
mexicana, inflorescences with tuber, runners and host members adnate to ovary; stylodia 2. Fruit a
root. B Rhopalocnemis phalloides, habit. (From Kuijt small, a 1-seeded achene.
1969, redrawn by J. Kuijt after Hooker 1856)
One sp., C. crassa Hook.f., Central and South
America from Costa Rica to Peru, in the Andes
Exorhopala Steenis, Hand. 6th Ned. Ind. Natuurwet. from 1,500 to 3,500 m alt. Parasitizing Composi-
Congr. 1931: 470 (1932); B. Hansen in Fl. Mal. I, 7: 790 tae and possibly bamboos.
(1976); Eberwein & Weber, Bot. J. Linn. Soc. 146: 513–517
(2004).
8. Ditepalanthus Fagerlind
Monoecious and protogynous yellow to orange- Ditepalanthus Fagerlind, Ark. Bot. Stockholm 29A, 7: 12,
red to brown red plants, arising from horizontal f. 1–5 (1938); B. Hansen, Flore de Madagascar 61: 4–6
slender (1–7 mm in diam.) stolon-like “runners” (1984).
which originate from a subspherical, central
tuber; peduncles leafless or at most with a few Monoecious and protogynous dark, bluish-black
much reduced inconspicuous bracts inserted at plants up to 20 cm high arising from an irregular,
the same level. Inflorescence bisexual, spadici- subspherical tuber; sheath around basal part of
form, sometimes at first breaking through the peduncle none or very inconspicuous; peduncle
tuber tissue which is lifted up with the upgrowing leafless. Inflorescences covered by peltate, hexag-
spadix, the latter covered by marginally cohering onal, eventually caducous bracts. Staminate flow-
hexagonal, peltate, caducous bracts. Flowers ers with a perianth of two tepals and a staminal
embedded in a dense layer of filiform hairs, the column ending in a globulous synandrium with
staminate ones with tubular, 3-lobed perianth 15–20 spherical locules in 2–3 layers; pistillate
and 3 stamens with at least partly distinct fila- flowers with a tubular perianth adnate to the
ments and a synandrium with 9–16 vertical ovary and surrounding the bases of the two
anthesis; staminate flowers with tubular, 4-

lobed perianth or splitting irregularly; stamens
connate into columnar synandrium with 20–30
locules in 2–3 superposed layers; pistillate flowers
surrounded by supporting hairs, with perianth
adnate to ovary and forming 2 low crests at the
top of the ovary alternating with the caducous
stylodia; stigmas capitate; ovary slightly com-
pressed in anterior/posterior direction. Fruit
narrowly oblong. Seeds globose.
One sp., R. phalloides Jungh., from India
through S China to Thailand and Vietnam, in
forest, up to 2,700 m alt.; parasitizing Euphor-
biac., Fagac., Legum., Morac., Theac. A second
species ascribed to this genus has been trans-
ferred to Ditepalanthus.
V. SUBFAM. SCYBALIOIDEAE Engl. (1889).
Peduncle and young inflorescence covered by tri-

angular bracts; flowers embedded in a dense layer
of filiform hairs; pollen grains pantopororate.
10. Scybalium Schott & Endl. Fig. 79
Scybalium Schott & Endl., Melet. Bot.: 3 (1832); B. Han-

Fig. 78. Balanophoraceae. Coryneaea crassa. A Habit.
B Staminate flower of var. crassa. C Same of var. sprucei. sen, Fl. Neotropica 23: 24–33, fig. 10–12 (1980).
(From Hansen 1980, redrawn from Hooker 1856 by
Victoria C.G. Friis) Monoecious or dioecious, red orange to rose pur-
ple or dark red to dark brown plants, 5–20 cm tall,
arising either directly from verrucose tubers or
stylodia; ovary 1-locular; stigmas capitate. Fruit from cylindrical, horizontal rhizome-like struc-
nut-like with a solitary seed. tures which originate from a central tuber. Ped-
One sp., D. malagasicus (Jumelle & uncle with triangular, more or less petiolate scaly
H. Perrier) Fagerlind, endemic to Madagascar, leaves. Inflorescences depressed-discoid to ovoid
up to 1,700 m alt. or almost cylindrical, at first covered by triangu-
9. Rhopalocnemis Jungh. Fig. 77 lar scaly bracts, each bract subtending an
extremely depressed unisexual or bisexual
Rhopalocnemis Jungh., Nov. Act. Ac. Caes. Leop.-Car. branch. Flowers embedded in a dense layer of
18, Suppl. 1: 213 (1841); B. Hansen in Fl. Mal. I, 7: 785 filiform hairs, staminate ones with a tubular,
(1976). 2–3-lobed perianth, the filaments connate into a
column, upwards often splitting into distinct fila-
Monoecious yellowish to brownish stout plants, ments and then again joining into a vertically (4)6
25–30 cm tall, arising from a large, irregularly (9)-locular synandrium; pollen grains panto-6
corrugated starchy tuber; sheath around base (8)-pororate; pistillate flowers compressed,
of peduncle well developed, irregularly lobed; perianth lobes 2, adnate to ovary; stylodia 2.
peduncle leafless or with low warts or slightly Fruit a small 1-seeded achene.
recurved, apparently spirally arranged scales. Four spp., Greater Antilles, Colombian and
Inflorescence spadiciform, unisexual or bisexual, Ecuadorean Andes, and SE Brazil. Parasitizing
at first covered by peltate scales which are shed at Legum., Melastomatac. and Myrsinac.
204 Balanophoraceae
Fig. 79. Balanophoraceae. A–E Scybalium fungiforme. A

One staminate inflorescence surrounded by several pistil-
late ones, all appearing from the same tuber. B Pistillate
flower. C Section of staminate inflorescence with two buds
and two kinds of trichomes. D Staminate flower. E Same,
longitudinal section, note pistillode. F–H Scybalium
depressum. F Habit. G Staminate flower. H Pistillate
flower. (From Hansen 1980, drawn by Victoria C.G. Friis,
A–E redrawn from Eichler 1869 and F from Hooker 1856) Fig. 80. Balanophoraceae. Lophophytum leandri. A
Tuber (at left the scar of the attachment to the host
root) and inflorescence in flower. B Staminate branch. C
VI. SUBFAM. LOPHOPHYTOIDEAE Engl. (1903). Two open anthers. D Pistillate branch. E Pistillate flower
and its subtending bract. (From Hansen 1980, drawn by
V.C.G. Friis)
Flowers in clavate panicles, usually perianthless,
not immersed in a layer of chaffy hairs; stylodia 2;
pollen grains 3-colporate. distinct, filaments short; anthers basifixed, longi-
tudinally 4-locular, dehiscing lengthwise; pollen
11. Lophophytum Schott & Endl. Fig. 80 grains psilate, prolate, tricolporate; pistillate
flowers sessile, densely arranged, prismatic, with
Lophophytum Schott & Endl., Melet. Bot.: 1 (1832); truncate top part, with or without an inconspicu-
B. Hansen, Fl. Neotropica 23: 45–54, fig. 19, 20 (1980). ous, 2-lobed perianth; stylodia 2, inserted in a
small cavity; stigmas capitellate. Fruit a small,
Monoecious brownish to maroon plants up to 1-seeded achene.
30 cm tall, arising from corrugated and often Three or four spp., Colombia, Peru, Bolivia, N
warty tubers of considerable size (up to 38 cm Argentina, Paraguay, Brazil (Acre and SE). Para-
diam.). Peduncle short or almost absent, covered sitizing Legum.
by triangular scaly leaves. Inflorescence once
branched, unisexual or bisexual, when young 12. Ombrophytum Poepp. ex Endl.
covered by angular-ovate bracts; bracts caducous,
subpeltate, pelta angular-ovate, each subtending Ombrophytum Poepp. ex Endl., Gen. Plant.: 73 (1836);
a branch, the pistillate branches below and stami- B. Hansen, Fl. Neotropica 23: 55–67, fig. 24–28 (1980) and
nate ones above. Staminate flowers with an in Acta Phytotax. Geobot. 33: 98 (1982).
inconspicuous, 2(1)-lobed perianth; stamens 2, Juelia Aspl. (1928).
Monoecious, whitish to pink or violet plants up to 14. Langsdorffia Mart.

20 cm tall, arising from subspherical, verrucose
tubers. Peduncle leafless, with a 2- or 3-lobed Langsdorffia Mart. in Eschw., J. Bras. 2: 179, t. 5 (1818);
sheath at the base. Inflorescence spadiciform, B. Hansen, Fl. Males. I, 7: 804–805 (1976) and in Fl.
once-branched, strictly female or with pistillate Neotrop. 23: 67–71 (1980); Cardoso et al., Syst. Bot. 36:
branches below and staminate branches above; 424–427 (2011), key.
bracts subtending the branches variously peltate, Dioecious, yellowish to wine-red plants up to 15
caducous. Staminate flowers up to 50 on a branch, cm tall, arising from buds on elongate (ca. 0.6 cm
without perianth; stamens 2, distinct, filaments thick) rhizome-like, pubescent, branched tuber,
short, anthers basifixed, 4-locular, dehiscing leaving a lobed sheath basally. Peduncles short or
lengthwise; pollen grains spheroid to prolate, tri- elongated, with numerous spirally arranged
colporate, pantocolpate; pistillate flowers about triangular lanceolate scaly leaves, the flower-
100 on a branch, without a perianth; ovary one- bearing apex flattish or slightly convex; staminate
celled, stylodia 2. Fruit a small, 1-seeded achene. flowers 3-merous with valvate tepals and the
Four spp., Ecuador (Santa Cruz, Galapagos stamens connate into a synandrium; anthers 3,
Islands), Peru, W Brazil, Bolivia, N Chile, NW horseshoe-shaped with the bend upwards; pollen
Argentina. Parasitizing Compos., Dioscoreac., grains (3)4(5)-zonoporate; pistillate flowers with
Legum., Solanac. tubular perianth; the single style exserted; ovary
apparently without cavity. Fruit a small, 1-seeded
13. Lathrophytum Eichl. achene.
Four spp., one from Mexico through C Amer-
Lathrophytum Eichl., Bot. Zeitung (Berlin) 26: 550, t. 9. ica and tropical South America to Brazil and
fig. 1–10, 12–15 (1868); B. Hansen, Bot. Tidsskr. 71: 77
Bolivia, one from SE Brazil, one from Madagascar
(1976) and in Fl. Neotrop. 23: 54–55 (1980).
and one from New Guinea. Parasitizing Elaeocar-
pac., Legum., Malpighiac., Meliac., Morac.,
Monoecious, probably yellowish to brownish Myrtac., Palmae, Sabiac.
plants up to 16 cm tall, arising from a subsphe-
rical tuber with a rough, warty surface. Peduncle 15. Thonningia Vahl Fig. 81
with a 2–3-lobed sheath appressed to its base,
leafless, glabrous or with a few peltate scales Thonningia Vahl, Skr. Naturhist.-Selsk. 6: 124, t. 6 (1810);
above and rudimentary branches. Inflorescence B. Hansen, Bot. Jahrb. 106: 359–377 (1986).
bisexual, spadiciform, when young covered by
rhombic or irregularly polygonate top parts of Dioecious (monoecious), bright red plants up to
peltate, early caducous bracts, during anthesis 20 cm tall, arising from rhizome-like, ca. 0.6 cm
completely devoid of bracts. Staminate flowers thick, horizontal, cylindrical, pubescent under-
in upper part of inflorescence, lacking perianth; ground tuber swollen to about 1.4–1.6 cm at
stamens 2; anthers sessile, 4-locular, dehiscing by points of contact with the host root; the peduncle
2 longitudinal slits; pollen grains suboblate, tri- gradually thickening into the hemispherical
colporate; pistillate flowers densely arranged on flower-bearing receptacle, both densely covered
slender branches, without perianth, stylodia 2. by imbricate, scaly, acute leaves. Flowers con-
Fruit a small, 1-seeded achene. cealed by the tips of the uppermost leaves,
One sp., L. peckoltii Eichl., SE Brazil, rarely ebracteate; staminate ones with 2–6 minute,
collected. Parasitizing Euphorb., Myristicac. apparently spirally arranged tepals; stamens 2–6,
connate into an elongated cylindrical, 8–24-
VII. SUBFAM. BALANOPHOROIDEAE Engl. (1889). locular synandrium; pollen grains (3)4(5)-porate,
slightly verrucate, similar to those of Langsdorf-
Plants contain wax-like substance; anthers con- fia; pistillate flowers densely packed but distinct,
nate into a synandrium; style solitary; pollen with a tubular perianth 3–4-lobed at the rim and a
zono-porate protruding style; ovary apparently 1-merous.
206 Balanophoraceae
Fig. 81. Balanophoraceae. Thonningia sanguinea. A

Plant with tuber and runners. B Staminate inflorescence,
longitudinally sectioned. C Pistillate inflorescence. D Sta-
minate flower. E Pistillate flower. F Same with fruit, Fig. 82. Balanophoraceae. Balanophora fungosa var.
longitudinally sectioned. (From Engler 1915) indica. Plant with staminate and pistillate inflorescences.
(From Kuijt 1969, redrawn by J. Kuijt after Hooker 1840)
Infructescence hemispherically enlarging. Fruit a
small, 1-seeded achene.
One sp., T. sanguinea Vahl, tropical Africa the monoecious species the staminate flowers
from Senegal to SW Ethiopia and southwards to either intermixed with pistillate ones or in a
Zambia. Parasitizing Apocynac., Euphorbiac., zone below or above the pistillate part. Staminate
Legum., Morac. flowers actinomorphic or slightly zgomorphic,
subtended by short, truncate bracts (sometimes
16. Balanophora J.R. & G. Forst. Fig. 82 rudimentary); tepals 3, 4–5 or 6 (14); anthers as
many and opposite the perianth segments, lack-
Balanophora J.R. & G. Forst., Char. Gen. Pl.: 99, t. 50 ing filaments and connate in a synandrium;
(1776); B. Hansen, Dansk Bot. Ark. 28 (1): 1–188 (1972) pollen grains spheroidal, (atrem), 3–4-zonopo-
and in Fl. Males. I, 7: 791–805 (1976). rate or 8–12-pantoporate; pistillate flowers
Cynopsole Endl. (1836). extremely small, lacking a perianth, inserted in
Acroblastum Soland ex Seem. (1866). great numbers among the club-shaped spadicles,
Balania Tiegh. (1896). and consisting only of the ellipsoid ovary and an
Polyplethia (Griff.) Tiegh. (1896).
elongated style. Fruit a minute, 1-seeded achene.
About 15 spp., tropical Africa, Comores,
Red, brown or yellow to yellowish-white plants Madagascar, temperate to tropical Asia, Malesia,
up to 30 cm tall, arising from subspherical or tropical Australia, Pacific Is. Parasitizing Acanth.,
cylindrical, often branched tubers; peduncles Acerac., Apocyn., Aquifol., Araliac., Asclep.,
leaf bearing; leaves 2–20, broad based, whorled, Berberid., Betulac., Celastr., Corylac., Datisc.,
opposite, distichous or spirally arranged; most Ebenac., Ericac., Euphorb., Fagac., Gramin.,
spp. dioecious and some monoecious or with Hamamel., Jugland., Laurac., Legum., Malvac.,
monoecious and dioecious individuals; some Morac., Myrtac., Oleac., Pinac., Piperac., Pittosp.,
spp. agamospermous. Inflorescence spadiciform, Rosac., Rutac., Stercul., Symploc., Theac., Urtic.,
apparently unbranched, unisexual or bisexual; in Verben., Vitac. Two subgenera: Subgen.
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Glossary
Bracteole see under prophyll. from the seedling’s radicular apex or

Calyculus a rim crowning the top of the ovary, nearly so. (2) Secondary haustorium:
usually considered a reduced calyx. a haustorium developed laterally
Cataphylls (1) Basal cataphylls: scale leaves from an epicortical root.
placed at the base of lateral Ligule a small flap of tissue at the inner base
branches. (2) Intercalary cataphylls: of some petals in Loranthaceae.
scale leaves interposed between suc- Monad a lateral inflorescence unit of a
cessive pairs of expanded leaves on a single flower, with or without brac-
percurrent shoot. teoles.
Cupule a cup-like structure, often formed by Passovian a dimorphic type of anther common
the fusion of foliar elements. in Passovia and some related genera,
Dyad a lateral inflorescence unit bearing with a prominent connective horn,
two lateral flowers, the median one the longer filaments often flattened
missing. and laterally excavated, accommo-
Epicortical a creeping root on the host surface, dating adjacent anthers.
root emerging from branches and/or the Pentad a lateral inflorescence unit bearing
base of the plant, bearing secondary five flowers; known only for Peri-
haustoria. stethium confertiflorum.
Fenestrae the preformed slits between petals into Percurrent continued longitudinal development
which avian pollinators insert their of a shoot.
beaks in order to open the flower. Prophyll one or two (often minute) foliar
Gland a cluster or plate of cells in the center organs flanking the base of a lateral
of a young haustorium above which axis. Especially in Loranthaceae, also
the penetrating (intrusive) organ referred to as (prophyllar) bracteoles.
differentiates; these cells eventually Ramal parasitism on the branches of a
undergo autolysis. parasitism host.
Haustorium (1) Primary haustorium: the intru- Triad a lateral inflorescence unit bearing
sive, absorptive organ developed one median and two lateral flowers.
DOI 10.1007/978-3-319-09296-6, # Springer International Publishing Switzerland 2015
Index
References to accepted names in bold-faced print, to synonyms in upright print, to illustrations in italics.
A B. subfam. Sarcophytoideae, 201 Dendrophthoe, 107, 111, 112

Acanthosyris, 150 B. subfam. Scybalioideae, 203 Dendrophthora, 179, 179
Acroblastum, 206 Barathranthus, 110 Dendrophthoraceae, 169
Actinanthella, 98, 99 Benthamina, 106 Dendrotrophe, 153
Aetanthus, 88, 88 Berhautia, 100 Desmaria, 90
Agelanthus, 98, 99 Brachynema, 130, 131 Diplatia, 107
A. sect. Acranthemum, 98 Buckleya, 152 Distrianthes, 111
A. sect. Agelanthus, 98 Ditepalanthus, 202
A. sect. Erectilobi, 98 C Douradoa, 188
A. sect. Longiflori, 98 Cansjera, 138 Dufrenoya, 154
A. sect. Obtectiflori, 98 Cathedra, 131, 132 Dulacia, 131, 132
A. sect. Purpuriflori, 99 Cecarria, 110
Agonandra, 138, 139 Cervantesia, 152 E
Alepis, 105 Cervantesiaceae, 143 Elytranthaceae, 73
Amphorogynaceae, 143 Champereia, 139 Elytranthe, 112
Amphorogyne, 151 Chaunochitaceae, 59 Emelianthe, 100
Amyema, 105, 110 Chaunochiton, 60, 61 Englerina, 100
A. sect. Tetrameri, 100 Chaunochitonaceae, 59 Engomegoma, 132
Amylotheca, 105, 110 Chlamydophytum, 201 Eremolepidaceae, 69
Anacolosa, 130, 130 Choretrum, 152 Erianthemum, 100
Anthobolus, 151 Cladocolea, 89 Eubrachion, 71
Antidaphne, 71, 71 Cladomyza, 153 Exocarpos, 154, 155, 156
Aptandra, 60, 60 Colpoon, 152 Exorhopala, 202
Aptandraceae, 59 Comandra, 153
Arceuthobiaceae, 169 Comandraceae, 143 F
Arceuthobium, 178, 179 Corynaea, 202 Furarium, 93
Arjona, 50, 151 Coryneaea, 203
Atkinsonia, 106, 106 Coula, 65, 66 G
Austroamericium, 164 Coulaceae, 65 Gaiadendraceae, 73
Curupira, 187, 188 Gaiadendron, 80, 90
B Cyne, 111 Geocaulon, 156
Bakerella, 99 Cynopsole, 206 Ginalloa, 180
Balania, 206 Ginalloaceae, 169
Balanophora, 206, 206 D Gjellerupia, 139
Balanophoraceae, 193 Dactylanthus, 200, 200 Globimetula, 100
B. subfam. Balanophoroideae, 205 Dactyliophora, 111
B. subfam. Dactylanthoideae, 199 Daenikera, 153 H
B. subfam. Helosidoideae, 201 Decaisnina, 106, 111 Hachettea, 199, 200
B. subfam. Lophophytoideae, 204 Dendromyza, 153 Harmandia, 61
B. subfam. Mystropetaloideae, 199 Dendropemon, 89 Harmandiaceae, 59
DOI 10.1007/978-3-319-09296-6, # Springer International Publishing Switzerland 2015
212 Index
Heisteria, 132, 133 Mida, 157 Phanerodiscus, 62

Helicanthes, 112 M. sect. Eucarya, 161 Phoradendraceae, 169
Helixanthera, 18, 101, 101, 112 Minquartia, 65, 66 Phoradendron, 181, 181, 182
Helosis, 201, 202 Misodendraceae, 121 Phragmanthera, 102, 102
Henslowia, 153, 154 Misodendrum, 122, 123, 124 P. sect. Eubracteatae, 102
Hondurodendron, 61 Moquiniella, 101 P. sect. Lepidotae, 103
Hylomyza, 154 Muellerina, 107 P. sect. Rufescentes, 103
Hyphear, 113 Myoschilos, 158 Phrygilanthus, 90
Myrtobium, 72 P. subgen. Quintralia, 96
I Mystropetalon, 199 P. subgen. Taguana, 90
Ileostylus, 107 Myzodendrum, 124 P. subgen. Tripodanthus, 96
Ixocactus, 94 Phthirusa, 89, 93, 94, 94
N P. sect. Dendropemon, 89
J Nanodea, 158, 158 P. sect. Passovia, 93
Jodina, 156, 157 Nanodeaceae, 143 Pilgerina, 160
Juelia, 204 Nestronia, 158 Plicosepalus, 103, 103
Notanthera, 90 Polyplethia, 206
K Notothixos, 181 Psathyranthus, 94
Korthalsella, 180, 181 Nuytsia, 18, 107, 108 Psittacanthaceae, 73
Kunkeliella, 157 Nuytsiaceae, 73 Psittacanthus, 31, 82, 94, 95
O P. subgen. Aetanthus, 88
L Ochanostachys, 66, 67 Ptychopetalum, 134
Lampas, 112 Octoknema, 126, 126 Pusillanthus, 95
Langsdorffia, 205 Octoknemaceae, 125 Pyrularia, 161
Lathrophytum, 205 Oedina, 101
Lepeostegeres, 113, 113 Okoubaka, 158, 159 Q
Lepidaria, 113, 114 Olacaceae, 127 Quinchamalium, 161
Lepidoceras, 72, 72 O. subfam. Dysolacoideae, 65
Lepionurus, 139 O. subfam. Dysolacoideae tribe R
Leptomeria, 157 Ximenieae, 187 Rhoiacarpos, 161
Ligaria, 91 Olax, 133 Rhopalocnemis, 203
Lophophytum, 196, 204, 204 Oliverella, 101 Rhopalopilia, 141
Loranthaceae, 73 Ombrophytum, 204 R. sect. Pentarhopalopilia, 141
L. subfam. Loranthoideae, 73 Omphacomeria, 159
L. subfam. Viscoideae, 169 Oncella, 101 S
Loranthus, 113 Oncocalyx, 102, 102 Santalaceae, 143
L. sect. Dendropemon, 89 O. sect. Longicalyculati, 102 Santalum, 161, 162
L. sect. Incrassati, 98 Ongokea, 62, 62 S. sect. Hawaiienisia, 161
L. sect. Infundibuliformes, 98 Opilia, 140, 140 S. sect. Mida, 157
L. sect. Notanthera, 91 O. subgen. Urobotrya, 141 S. sect. Polynesica, 161
L. sect. Oryctanthus subgen. Opiliaceae, 137 S. sect. (Eu)Santalum, 161
Paryctanthus, 91 Oryctanthus, 91, 92 Sarcophyte, 201, 201
L. sect. Phrygilanthus subsect. Oryctina, 92 Sarcopodaceae, 154
Metastachys, 96 Oryctina, 91 Sarcopodales, 154
L. sect. Psittacanthus, 94 Osyridicarpos, 159 Sarcopus, 154
L. sect. Tetrameri, 100 Osyris, 159 Schoepfia, 167
L. subgen. Erianthemum, 100 O. sect. Acanthosyris, 150 Schoepfiaceae, 167
L. [unranked] Struthanthus, 95 Scleropyrum, 162, 162
Loxanthera, 113 P Scorodocarpus, 134, 134
Lysiana, 107 Panamanthus, 92 Scurrula, 115
Papuanthes, 115, 115 Scybalium, 203, 204
M Passovia, 93, 93 Septulina, 103
Maburea, 133 Pedistylis, 102 Socratina, 103
Macrosolen, 114, 114 Pentarhopalopilia, 141 Sogerianthe, 115, 115
Malania, 189 Peraxilla, 108 Spirogardnera, 163
Maracanthus, 91 Peristethium, 93 Spirostylis, 95
Melientha, 140 Phacellaria, 160, 160 Spragueanella, 104
Index 213
Staufferia, 163 Thaumasianthus, 116 U

Strombosia, 134, 135 Thesiaceae, 143 Urobotrya, 141
Strombosiopsis, 135 Thesidium, 163
Struthanthus, 95, 96 Thesium, 164 V
Thonningia, 205, 206 Vanwykia, 104
T Tolypanthus, 116 Viscaceae, 169
Tapinanthus, 104 Trilepidea, 108 Viscum, 171, 182, 183
Taxillus, 104, 116, 116, 160 Tripodanthus, 96, 96
T. sect. Bakerella, 99 Tristerix, 96, 97 X
T. sect. Septulina, 103 Trithecanthera, 117 Ximenia, 189, 189
Tetrastylidium, 135 Tupeia, 108 Ximeniaceae, 187

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Edited by K.

XII Flowering Plants Eudicots

Job Kuijt Bertel Hansen

Prof. Dr. Klaus Kubitzki

ISBN 978-3-319-09295-9 ISBN 978-3-319-09296-6 (eBook)

Library of Congress Control Number: 2014949618

# Springer International Publishing Switzerland 2015

Printed on acid-free paper

Springer is part of Springer ScienceþBusiness Media (www.springer.com)

Hamburg, 16 August 2014 Klaus Kubitzki

I am indebted to Valéry Malécot for information on Brachynema and Scleropyrum, to

Sleumer, H. 1935a. Olacaceae. In: Engler, A., Prantl, K., http://2008.botanyconference.org/engine/search/index.

Chromosome Numbers. A listing of known chro- The embryology of Loranthaceae forms a

(Helixanthera ligustrina), it eventually finds itself

that—as in most Loranthaceae—the resultant fragmentary information be thought to be repre-

opment. Direct contact with the vascular system

The Austrian mystic and educator Rudolf

Abies, Larix, Picea, Tsuga, and especially many References

Olacaceae ovule reduction, we may perceive convincing,

References adendron). II. The photosynthetic capacity of mistle-

POLLEN. The pollen of Aptandra is heteropolar and

KEY TO THE GENERA OF APTANDRACEAE

1. Stamens united in a tube surrounding the style 2

nearly spherical, at the tip of the filament, and

Harmandia Pierre ex Baillon, Bull. Soc. Linn. Paris 2: 770

Trees with distichous, lanceolate leaves.

2. Chaunochiton Benth. Fig. 6 Dioecious trees to 12 m high, young shoots

triangular in polar view, tricolporate, the colpi

Phanerodiscus Cavaco, Notul. Syst. (Paris) 15: 11 (1954).

Fig. 9. Coulaceae. Minquartia guianensis. A Branch with

Trees, said to be autotrophic (Ping 1997). Young

Fig. 10. Coulaceae. Ochanostachys amentaceae. A Flower-

KEY TO THE GENERA OF EREMOLEPIDACEAE

1. Leaves of adult plants squamate and peltate

1. Antidaphne Poepp. & Endl. Fig. 11

Antidaphne Poepp. & Endl., Nov. Gen. Sp. Pl. 2: 70 (1838).

Leafy plants with alternate phyllotaxy even when

APG, 1998. An ordinal classification for the families of

many extant Cladocolea species. The addition of F L O R A L S T R U C T U R E . The flowers of Lorantha-

It is scarcely surprising that the haustorial

that may be 40–50 cm in diameter in Psitta- E V O L U T I O N . Diversification and aerial parasit-

C O N S E R V A T I O N . The importation of opossums 2. Petals bright yellow, nearly 40 cm long, turning

13. Anthers basifixed or nearly so, often “Passovian”;

anthers with acicular tips, and by its consistently

2. Cladocolea Tiegh. Fig. 16

Cladocolea Tiegh., Bull. Soc. Bot. France 42: 166–168

Plants of moderate size, glabrous to short-pubes-

Dendropemon (Blume) Reichenb., Rept. Herb.: 73 (1841);

copious, whitish endosperm; viscin developed

Desmaria Tiegh., Bull. Soc. Bot. France 42: 458–459

Large mistletoes with long epicortical roots

dicotylous, with massive cotyledons and promi-

10. Oryctina Tiegh.

Oryctina Tiegh., Bull. Soc. Bot. France 42: 168–169 (1895);

Leafy plants of moderate size, at least some

11. Panamanthus Kuijt

Panamanthus Kuijt, Ann. Missouri Bot. Gard. 78: 172–176

Scandent plants of Struthanthus-like habit,

viscin tissue. Embryo small, slender, dicotylous,

12. Passovia Karsten Fig. 19

Passovia Karsten, Bot. Zeit. 4: 107 (1846); Kuijt, Plant Div.

Leafy, percurrent plants, glabrous or with partly/

triads. Flowers hexamerous or tetramerous

14. Phthirusa Mart. Fig. 20