Received: 24 November 2021
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Revised: 5 April 2022
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Accepted: 18 May 2022
DOI: 10.1111/btp.13130
REVIEW
Consuming and consumed: Biotic interactions of African
mistletoes across different trophic levels
Yuliya Krasylenko1
| Tonjock Rosemary Kinge2,3
| Yevhen Sosnovsky4
Natalia Atamas5
| Katamssadan Haman Tofel2
| Oleksii Horielov6
|
3
Gerhard Rambold
1
Department of Biotechnology, Faculty
of Science, Palacký University Olomouc,
Olomouc, Czech Republic
Department of Biological Sciences,
Faculty of Science, The University of
Bamenda, Bambili, Cameroon
2
Department of Mycology, University of
Bayreuth, Bayreuth, Germany
3
Botanical Garden, Ivan Franko National
University of Lviv, Lviv, Ukraine
4
Laboratory of Population Ecology,
Department of Animal Monitoring and
Conservation, I.I. Schmalhausen Institute
of Zoology, National Academy of Science
of Ukraine, Kyiv, Ukraine
5
Department of Dendrology, M.M.
Gryshko National Botanic Garden,
National Academy of Sciences of Ukraine,
Kyiv, Ukraine
6
Correspondence
Tonjock Rosemary Kinge, Department of
Biological Sciences, Faculty of Science,
The University of Bamenda, P.O.Box 39
Bambili, NW Region, Cameroon.
Email: rosemary.tonjock@uni-bayreuth.de
Funding information
Alexander von Humboldt-Stiftung, Grant/
Award Number: George Foster Fellowship
for Experienced researche; European
Regional Development Fund (ERDF)
project, Grant/Award Number: CZ.02.1.0
1/0.0/0.0/16_019/0000827; Private joint
stock company (PJS) “Carlsberg Ukraine”
(Kyiv, Ukraine)
Associate Editor: Ferry Slik
Handling Editor: Nico Bluthgen
|
Abstract
Mistletoes, as perennial hemiparasitic angiosperms that parasitize woody plants, are
an important component of the highly diverse, endemically rich and mosaic African
flora, which is attributed to the Holarctic, Paleotropical, and Cape Floristic kingdoms.
The richness of African mistletoes from the Loranthaceae and Viscaceae, along with
many aspects of their biology and ecology, was covered in the comprehensive monograph of Polhill and Wiens (1998, Mistletoes of Africa, Royal Botanic Gardens). The
present review is devoted to the taxonomic and functional diversity of symbionts
associated with mistletoes in Africa and adjacent islands that contribute to the major
biological functions of mistletoes, such as establishment and growth, nutrition and fitness, resistance to external stresses, as well as pollination and dispersal. These functions are favored by more or less distinct sets of associated bionts, including host
plants, animal herbivores, frugivorous birds, nectar- and pollen-feeding insects, and
endophytic microorganisms. A separate section is devoted to mistletoe epiparasitism
as a special case of host selection. All these organisms, which are components of the
mistletoe-associated community and multitrophic network, define the role of mistletoes as keystone species. Some aspects of the symbiont communities are compared
here with patterns reported for mistletoes from other continents, particularly to identify potential relationships that remain to be explored for the African species. In addition, properties of endophytic mistletoe associates that contribute to the plant's
communication with coexisting organisms are considered. We also highlight the important gaps of knowledge of the functioning of mistletoe-associated communities in
Africa and indicate some applied issues that need future attention.
Abstract in French is available with online material.
KEYWORDS
dispersers, frugivores, hemiparasites, host plant, host preference, microbiome, pollinators,
vectors
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2022 The Authors. Biotropica published by Wiley Periodicals LLC on behalf of Association for Tropical Biology and Conservation.
Biotropica. 2022;54:1103–1119.
wileyonlinelibrary.com/journal/btp
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I NTRO D U C TI O N
Helixanthera and all Viscaceae develop bark strands, similarly to
some members of the genera Oncocalyx (sections Longicalyculati and
The term “mistletoe” refers to a functionally well-defined yet poly-
Oncocalyx), Agelanthus (sections Erectilobi and Purpureiflori), Oedina,
phyletic group of aerial plant hemiparasites that share common life
and Spragueanella (Calvin & Wilson, 1998; Kuijt & Hansen, 2015). In
history traits, such as rootless habit, a specific type of biotic inter-
general, the external haustorium morphology may vary in the same
actions with the host plants, host-dependence, cryptic mimicry of
mistletoe species depending on the host plant, whereas the devel-
host plants, and the presence of a specialized organ, the haustorium,
opmental process is more conserved, allowing for a more precise
for gaining water and nutrients from the host (Kuijt & Hansen, 2015;
differentiation of haustorium types (L. Teixeira-Costa, pers. comm.).
Okubamichael et al., 2016). Mistletoes occur on all continents
No information is currently available as to haustorium structure in
except Antarctica and represent several families in the order
Berhautia and Socratina (Loranthaceae).
Santalales, especially Loranthaceae (ca. 900 species) and Viscaceae
Populations of some African mistletoes are reportedly declining
(ca. 500 species), but also some Santalaceae, Amphorogynaceae,
(Polhill & Wiens, 1998). For instance, of the 11 occurrences of epipar-
and Misodendraceae (Nickrent et al., 2010).
asitic mistletoes reported by Soyer-Poskin and Schmizt (1962) from
The African flora is dominated by tropical and subtropical ele-
a locality in the Democratic Republic of the Congo, no epiparasite
ments belonging to different biomes (e.g., savanna, fynbos, des-
and few likely habitats remained by 2015 (Wilson & Calvin, 2017).
ert, Nama, Succulent Karoos, deciduous, and evergreen forests)
Habitat transformation and overharvesting by humans have been
that have evolved in isolation and includes numerous biodiversity
reported as major drivers of decline of some mistletoe species in
hotspots (such as the Сape Floristic Region) with remarkable occur-
the Mascarene Islands and Seychelles, while the near-extinction of
rences of endemics (Klopper et al., 2006). African mistletoes (includ-
Bakerella hoyifolia subsp. bojeri on Reunion was attributed to the loss
ing those on adjacent islands) are represented by Loranthaceae (258
of its hypothetically main dispersers (flying foxes, doves, and parrots)
species from 23 genera) and Viscaceae (81 species from 3 genera)
since human colonization of the island (Albert et al., 2017). Many
(see Table S1), both of which have a presumed Gondwanan origin but
species of African mistletoes are being studied by ethnobotanists
apparently different dispersal histories. The Loranthaceae presum-
due to their traditional use in spiritual practices as well as increasing
ably spread from Asia across the Northern Hemisphere to mainland
exploitation in officinal medicine and by herbalists as “all-healing,”
Africa in the Eocene (Grímsson et al., 2018; Liu et al., 2018), whereas
“bone-setting,” and “fertility-boosting” drugs (Koffi et al., 2020;
the major African genus of Viscaceae, Viscum, probably originated
Oriola et al., 2020). At the same time, due to their broad host range
in Africa in the Eocene, followed by dispersal to other continents
and tendency to spread rapidly, many mistletoe species have gained
and a later colonization of northern Saharan Africa from continen-
a reputation as notorious pests that cause significant losses in tree
tal Asia (Maul et al., 2019). Mistletoes on islands neighboring Africa
crops (Dibong et al., 2008).
(i.e., Madagascar and Western Indian Ocean islands) may have ar-
Nevertheless, mistletoes play a crucial role in ecosystems as
rived at their present location by dispersal from the continent, as
secondary foundation species, providing key resources such as
has been hypothesized for Socratina and Viscum species (Maul
substrate and microhabitat for microorganisms and arthropods
et al., 2019; Vidal-Russell & Nickrent, 2008). In addition, Bakerella
(Peršoh, 2013; Zamora et al., 2020), a food source for herbivores
(currently found on Madagascar, Mascarenes, and Seychelles) and
(Těšitel et al., 2021; Watson & Herring, 2012), and a nesting site
Korthalsella (with patchy distribution across South-Eastern Asia to
for birds (Cooney et al., 2006; Ndagurwa et al., 2016; Těšitel
Australia, Pacific and Indian oceans, and Eastern Africa) could hypo-
et al., 2021; Watson & Herring, 2012). Consequently, mistletoes
thetically have spread from South or South-Eastern Asia via a south-
contribute to the symbiotic communities of their hosts by increas-
ern hemisphere route, for example, by vicariance during the breakup
ing the total load of microbial associates, inquilines, herbivores,
of Gondwana or by steppingstone and long-distance dispersal path-
pollinators, and dispersers, bringing an array of other associated
ways (Molvray et al., 1999; Polhill & Wiens, 1998).
guilds including predators, parasites, and parasitoids (Zamora
Based on the haustorial anatomy and development in African mis-
et al., 2020). Studies in the northern temperate regions have
tletoes, 14 haustorium types are known that are divided into 4 basal
empirically demonstrated mistletoes promoting the diversities
types with at least 3 subtypes: woodroses, epicortical roots, clasping
of endophytic fungi (Peršoh, 2013; Peršoh et al., 2010), arthro-
unions, and bark strands (Calvin & Wilson, 1998). Woodrose-forming
pods (Lázaro- González et al., 2017, 2020; Zamora et al., 2020),
mistletoes include some representatives of Erianthemum, Moquiniella,
and frugivorous birds (Mellado & Zamora, 2016) in the host-tree
Pedistylis, Tapinanthus (Loranthaceae), and Viscum (Viscaceae)
canopies. In addition to the direct mistletoes' input to biodiver-
(Calvin & Wilson, 1998; Dzerefos et al., 1998, 2003). In turn, epi-
sity, modifications in the host plant metabolome in response to
cortical roots occur in the mistletoe genera Bakerella, Helixanthera,
permanent mistletoe parasitism impose selective pressure on
Plicosepalus, Taxillus, and Vanwykia (Calvin & Wilson, 2006),
associated communities (Lázaro- González et al., 2021), trigger-
whereas clasping unions characterize Actinanthella, Emelianthe,
ing cascading responses in ecosystems. Mistletoes can therefore
Englerina, Globimetula, Oedina, Oliverella, Oncella, Phragmanthera,
exert an ambivalent effect on host plants by facilitating their
Septulina, Spragueanella, and Oncocalyx section Oncocalyx (Calvin
reproduction through the attraction and permanent support of
& Wilson, 1998, 2006). According to Teixeira-Costa et al. (2020),
shared generalist pollinators and vectors (Těšitel et al., 2021), but
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KRASYLENKO Et AL.
1105
at the same time reducing the physiological fitness of the hosts
associations since Balle (1964a, 1964b) and Philcox (1982), except
by depletion of their water and nutrient supplies and increasing
for occasional studies dealing with individual mistletoe taxa (Albert
susceptibility to pathogens and herbivores (Griebel et al., 2017).
et al., 2017). Here, we discuss host diversity and patterns of host
Furthermore, community-level impacts of mistletoes are seen be-
use in the African mainland and island mistletoes based on historical
yond their hosts through the production of nutrient-rich litter that
and recently published data supplemented with herbarium specimen
enhances host litter decomposition and contributes to carbon and
records retrieved from various online databases and digitized her-
nutrient fluxes in ecosystems (Ndagurwa et al., 2020), as well as
barium specimens. Our data set (Table S1) includes over 1000 host
attraction of seed dispersers that bring in and deposit (as excreta)
plant species from 553 genera, 119 families, and 40 orders recorded
the seeds of other plants, promoting increased plant diversity
for 313 mistletoe species (plus 25 infraspecific taxa) from 26 genera.
in forests (Těšitel et al., 2021). These effects, when combined,
Host species data are still lacking for 39 mistletoe taxa (26 species
facilitate changes in the composition of soil microbiota, vegeta-
and 13 infraspecific taxa), requiring further studies.
tion, and associated herbivore fauna beneath parasitized trees,
Host preferences in mistletoes are reputedly dynamic and at-
leading to long-term vegetation shifts and habitat restructuring
tributed to several factors such as host morphology defining the
(Hódar et al., 2018; Mellado et al., 2016; Mellado & Zamora, 2017;
compatibility with a mistletoe's haustorium, physiological fitness
Ndagurwa et al., 2014; Watson & Herring, 2012). Current under-
and nitrogen content determining the host's “quality,” as well as
standing of the top-down and bottom-up effects of mistletoes
host abundance and stability in an ecosystem crucial for the du-
within symbiotic networks is still at an early stage, and more em-
ration of mistletoe-host contact (Gairola et al., 2013; Norton &
pirical data at finer levels (individuals and populations) both in the
Carpenter, 1998; Polhill & Wiens, 1998; Teixeira-Costa et al., 2020).
spatial and temporal contexts are required to make broad-scale
In Africa, most mistletoe's host plants belong to the core eudicoty-
inferences.
ledons, with the greatest mistletoe diversity confined to host fam-
Presently, little is known about the composition and function
ilies such as Fabaceae, Malvaceae, Euphorbiaceae, Rubiaceae, and
of the organisms associated with mistletoes in Africa (Figure 1).
Combretaceae that are central to the African flora and contain nu-
In this review, we summarize existing knowledge on this topic,
merous woody species with diverse habitat requirements (Figure 2).
highlight major gaps to be filled, and identify challenges for fu-
Gymnosperms, Magnoliids, and monocots are occasionally parasit-
ture research. Due to the complicated biogeography of some
ized by promiscuous mistletoe species, with the exception of Pinus
African mistletoe taxa, the geographic scope of this review in-
and Juniperus, which host some specialized taxa from the Viscaceae
cludes mainland Africa with its neighboring islands to the west (in
(Table S1). On the genus level, Combretum and Ficus host the greatest
the Gulf of Guinea) and east (Madagascar, Comoros, Mascarenes,
mistletoe diversity, with 72 and 62 mistletoe species, respectively
and Seychelles). We organize our review by discussing symbiont
(Figure S1), whereas nearly 35% of the host genera are associated
guilds with different trophic positions relative to mistletoes, and
with only one mistletoe species. Fossil pollen evidence indicates that
in regard to their roles in mistletoe function. First, through an
many of the host families of extant mistletoes (including some of
analysis of published and herbarium data, we address patterns
those listed above) were available as potential hosts for African mis-
of host preference in mistletoes that contribute to their growth,
tletoes in the early Miocene (Grímsson et al., 2018), suggesting long-
distribution, and speciation. The following sections are devoted
term relationships between present-day mistletoe species and these
to mistletoe consumers and such reproduction-associated symbi-
host families. Patterns of host use by mistletoes, such as the relative
onts as pollinators and dispersers. We then discuss the diversity
number of specific host taxa within the overall host range and the
and composition of endophytic mistletoe associates, emphasizing
host overlap, vary across mistletoe genera. The high proportion of
their contribution to the role of mistletoes as interaction “hubs” in
specific host taxa (e.g., families and genera) may reflect significant
ecological networks. Finally, we touch upon some applied aspects
niche differentiation and geographic isolation of mistletoes (this may
of symbiotic interactions in mistletoes that require more attention
apply to the genera occurring on islands: Bakerrela, Korthalsella, and
in the future.
Viscum) or the presence of highly indiscriminate species that act as
opportunists (e.g., in Erianthemum and Tapinanthus) (Figures 2 and
2 | H OS T S O F A FR I C A N M I S TLE TO E S :
D I V E R S IT Y A N D A S S O C I ATI O N PAT TE R N S
S2). Such opportunistic species seem to be also the main contributors
to the considerable host overlap between Agelanthus, Erianthemum,
Globimetula, Phragmanthera, and Tapinanthus, and between these and
the other mistletoe genera (Figure S3). In Viscum, the increased host
Following the last comprehensive assessment of host associations
overlap with other mistletoes likely stems from the high richness and
in African mistletoes by Polhill and Wiens (1998, 1999a, 1999b) and
ecological/geographic differentiation of species. Arceuthobium and
a number of regional studies (see Table S1 for the reference list),
Taxillus appear segregated from the other African mistletoe genera
Grímsson et al. (2018) have recently compiled the continent-wide
due to the lack of shared host species (Figure S3). These two genera,
published host species records for the African Loranthaceae. In con-
along with Korthalsella, have their main distribution ranges outside
trast, the island mistletoe taxa (from the Madagascar and neighbor-
Africa (Polhill & Wiens, 1998) and thus may be distantly related to
ing islands) have remained virtually unaddressed in terms of host
other African mistletoes. Liu et al. (2018), however, speculated that
1106
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KRASYLENKO Et AL.
F I G U R E 1 Diversity of biotic
associations of African mistletoes.
Indications: straight lines—well-studied;
dashed lines—scarcely studied; dotted
lines—still unstudied. Graphical drawing
by Natalia Pendiur
the only African species of Taxillus, T. wiensii, has derived from a local
species-level host specificity trends and host overlap among mis-
lineage rather than from the rest of Taxillus residing in Asia.
tletoes, geographic patterns (as many African plant genera contain
Much of the available host records are at the genus and fam-
both narrow- and broad-ranged species whose distributions over-
ily ranks (Table S1), making it difficult to accurately assess host
lap), and recently revised taxa that have undergone changes to es-
preferences in mistletoes. This is especially true when assessing
tablished names. As arguably the most striking example of the latter,
F I G U R E 2 Host associations of mistletoes in Africa at the family level, based on data in Table S1. Host plant classification follows
Stevens (2001 onwards), The Angiosperm Phylogeny Group (2016), and Ran et al. (2018), and the coloring of major plant clades follows Byng
et al. (2018). Classification of the Santalales (including hosts and mistletoes) follows Kuijt and Hansen (2015). No. sp. indicates (horizontally)
the number of African mistletoe species in each genus and (vertically) total number of host-plant species in each family (including hybrids but
excluding infraspecific taxa such as subspecies and varieties) recorded for these mistletoes in Africa and adjacent islands. In all calculations,
familial and generic host records (those with “sp.” in Table S1) were omitted when identified subordinate plant taxa (genus or species,
respectively), were additionally present among hosts for a given mistletoe taxon; otherwise, all “sp.” records of a family or genus were
counted as one “species.” Host families with some records of taxa introduced to Africa are marked with “*,” and those containing introduced
host records only are marked with “**”. Mistletoe genera are listed alphabetically and by family as follows: Ac Actinanthella, Ag Agelanthus,
Ba Bakerella, Be Berhautia, Em Emelianthe, En Englerina, Er Erianthemum, Gl Globimetula, He Helixanthera, Mo Moquiniella, Oe Oedina, Ol
Oliverella, On Oncella, Onc Oncocalyx, Pe Pedistylis, Ph Phragmanthera, Pl Plicosepalus, Se Septulina, So Socratina, Sp Spragueanella, Tap
Tapinanthus, Tax Taxillus, Va Vanwykia, Ar Arceuthobium, Ko Korthalsella, Vi Viscum
KRASYLENKO Et AL.
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Acacia serves as key host for numerous African mistletoe species
Helixanthera and Korthalsella) presumably include components with
but is treated sensu lato in many host records due to only recent
distinct dispersal histories and of independent, relatively recent
reclassification of the genus, which placed all the African taxa into
South Asian origin (Grímsson et al., 2018; Liu et al., 2018; Molvray
Senegalia and Vachellia (Kyalangalilwa et al., 2013). Extraction of spe-
et al., 1999; Polhill & Wiens, 1998). Overall, our compiled records
cies records of Acacia s.str. (most of which have been introduced
(Table S1) do not indicate a consistent preference trend for island
into the area covered in this review) shows that these plants are
versus mainland mistletoes, with significant overlap in their general
common hosts for Globimetula, Phragmanthera, and Tapinanthus mis-
host ranges at the genus level. Island mistletoes apparently avoid
tletoes, whereas the two above-mentioned indigenous genera are
some host families that are widely distributed and usually preferred
apparently preferred by Plicosepalus, Tapinanthus, and some Viscum
by mainland mistletoe species, such as Combretaceae and Fabaceae.
species (Table S1).
Conversely, in families associated exclusively with island mistletoes
Generalist mistletoes (i.e., with broad host specificity and no
(Cunoniaceae, Escalloniaceae, Menispermaceae, Sarcolaenaceae,
clear preference; associated with three and more host families) ac-
and Winteraceae), most of the records pertain to host taxa that
count for most of the total host diversity recorded, although rela-
are endemic to the islands but parasitized by generalist mistletoes.
tively few of them (some Agelanthus, Erianthemum, Globimetula,
The exception is Sarcolaenaceae, where half of the host records are
Phragmanthera, and Tapinanthus) have a very broad host range of
of specialists. Furthermore, island endemics appear to also prevail
more than 50 plant species (up to 181 in Tapinanthus globiferus;
among all host species recorded exclusively for island mistletoes (ca.
Table S1). About 42% of all mistletoe taxa with host records appear
60 species from 34 families that constitute half of the island host
to be specialists, assigned here to several categories: (1) mistletoes
records, the rest being mostly at the genus level and from genera
that occur on multiple host species of two families with unclear pref-
that occur both on the island and on mainland Africa, such as Erica,
erence and regarded as potential specialists (35.5% of all specialists);
Eugenia, and Symphonia). However, whether the specialist mistletoes
(2) family specialists that are associated with one to several host
target local endemics or more widespread congeneric species as
families but clearly prefer hosts of one family or genus (16.3%); and
hosts remains unclear, as many of these mistletoes' host records are
(3) strict specialists that have only one to several records on plants
at the genus level. Nevertheless, the above evidence suggests that
of a single genus (48.2%). Among the major mistletoe genera, the
island mistletoes favor local narrowly restricted host lineages over
proportion of specialists is highest in Plicosepalus (primarily special-
widespread species that extend to mainland Africa. The widespread
ized on fabaceous hosts), followed by Helixanthera, Bakerella, Viscum,
species (e.g., Ceriops tagal and Aphloia theiformis) and the introduced
Erianthemum, and Agelanthus, whereas the prevailing majority of
crops are usually shared as hosts by the generalist island mistletoes
Oncocalyx, Tapinanthus, and Phragmanthera species are generalists
with their mainland relatives.
(Figure S2). Although these patterns are predominantly consistent
In Viscum, the differentiation in host preference between main-
with those reported by Polhill and Wiens (1998), they may be some-
land and island is most apparent: almost twice as many strict spe-
what compromised by limited data from poorly studied species and
cialists are present among island taxa (about 37% of all Viscum taxa
the lack of frequency data for each mistletoe-host pair. In addition,
with host records; Table S1) as among their mainland relatives, al-
generalist mistletoes may exhibit regional host specialization, a phe-
though the proportion of all specialists is nearly equal in the two
nomenon often attributed to the occurrence of intraspecific races in
groups. Furthermore, of all host genera associated with Viscum, ca.
mistletoes, as has been documented for some species of Agelanthus,
16% (32 genera) are recorded only for island mistletoes, and only
Erianthemum, Phragmanthera, Tapinanthus, and Viscum in Africa
9.4% are common to both island and mainland Viscum. However,
(Gairola et al., 2013; Okubamichael et al., 2014; Okubamichael,
about half of the former genera are not endemic to the islands but
Griffiths, & Ward, 2011; Polhill & Wiens, 1998). Furthermore, mis-
include species that are either parasitized by mainland non-Viscum
tletoe occurrence on a particular host may depend on factors other
mistletoes (such as Acalypha, Dalbergia, Vernonia, and Uapaca) or
than host preference, such as microclimatic conditions (which are
do not have mistletoe associations on the mainland (e.g., Bruguiera,
critical for mistletoe germination and establishment), dispersal con-
Cerbera, Cryptocarya, and Hirtella). Most of the records of specialist
straints (feeding habits of dispersers, lack of suitable vectors, or low
island Viscum refer either to endemic host genera (e.g., Oncostemum,
fruit palatability), or mistletoe consumption by herbivores. Finally,
Xerochlamys), endemic species of more widespread genera (such as
the remarkable ability of some generalist mistletoes to mimic their
Brachylaena merana and Neocussonia bojeri from Madagascar), or
preferred hosts in leaf shape, texture, and color (e.g., as a concealing
widespread genera known to contain species endemic to the islands
strategy to avoid consumption by herbivores; Polhill & Wiens, 1998;
(Croton and Erica). Following Maul et al. (2019), the above patterns
Dibong et al., 2008) may contribute to observation bias (i.e., over-
suggest that geographic isolation is the main driver of host prefer-
looking by humans).
ence shifts in African mistletoes, with novel lineages likely deriving
Island mistletoe taxa (from Madagascar and the western Indian
Ocean islands) show higher overall host specificity compared to
from generalist species through niche shifting promoted by both migrant and local dispersers.
mainland ones (Figure S2). However, this trend may be confounded
Approximately 13.5% of all host taxa recorded for African mistle-
by the unresolved phylogenetic and phylogeographic relation-
toes are introduced species from other continents (Table S1). Most
ships of the mistletoe genera discussed here, some of which (e.g.,
of these are from families that also comprise many native host plants,
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KRASYLENKO Et AL.
1109
such as Fabaceae (25 introduced host species), Euphorbiaceae (10),
and Malvaceae (8) (Figure 2), implying an increased predisposition
of mistletoes to these plant families. Mistletoe diversity is particularly high in species grown either as large trees or in dense plantations (e.g., Hevea brasiliensis, Persea americana, Psidium guajava,
Theobroma cacao, species of Citrus and Prunus), probably due to the
frequent visits by certain guilds of birds (such as woodland species,
habitat generalists, and migrants; Bennett et al., 2021) and other
mistletoe vectors. Generalist species of Agelanthus, Erianthemum,
Globimetula, Phragmanthera, and Tapinanthus are the main users of
introduced plants, both in terms of numbers of mistletoe and host
species involved in these interactions (Figure S4). Nevertheless,
these mistletoe genera differ greatly as to their propensity to form
novel host associations (expressed here as an “opportunism” index,
based on the proportion of species within each mistletoe genus that
parasitize introduced hosts), which is the highest in Tapinanthus and
Globimetula and lowest in Helixanthera and Plicosepalus (Figure S4).
The share of generalist mistletoe species in each genus, however,
only partly explains the above trend, given that some mistletoes regarded as potential or family specialists (e.g., Agelanthus flammeus,
Bakerella gonoclada, and Erianthemum melanocarpum) also employ
introduced species as hosts while many generalist mistletoes apparently avoid them (Table S1). In this respect, of particular interest are
F I G U R E 3 Occurrence of mistletoe epiparasitism on other
mistletoes (green blocks) and root-parasitic plants (light-brown
blocks) in Africa. Numbers under “parasites” indicate the total
number of species in each genus recorded to act as epiparasites
and the subtotal of species parasitizing other mistletoes, and those
under “hosts” indicate the number of epiparasitic mistletoe species
hosted by members of each host genus. Different line patterns
are given for clarity. Mistletoe genera not involved in epiparasitic
interactions are not shown
species recorded primarily or exclusively on introduced hosts (e.g.,
Agelanthus guineensis on Citrus sp. and Viscum ceibarum on Ceiba
on Loranthaceae and Loranthaceae epiparasitic on Loranthaceae,
pentandra), suggesting that they may have broader yet undocu-
both in Africa (Figures 2 and 3) and globally (Wilson & Calvin, 2017).
mented host ranges or have specialized on local archaeophytes as
The majority of African species are facultatively epiparasitic gener-
hosts. In addition, numerous species widely cultivated in Africa have
alists (Table S1), which is also true at the global level (Krasylenko
their natural range in some parts of the continent or adjacent islands
et al., 2021; Wilson & Calvin, 2017). Obligate epiparasitism occurs in
(all treated here as “native”), and many of these (indigenous acacias
two African Viscum species—V. goetzei, parasitizing solely an Englerina
as well as Coffea, Ficus, Nerium, Syzygium) serve as important hosts
host, and V. loranthicola, associated with a number of Loranthaceae
for some generalist and specialist mistletoe species (Table S1). The
host genera—and has also been suspected for Agelanthus dichrous
introduction and artificial expansion of the range of plant species
being highly selective towards Loranthaceae hosts (Wilson &
suitable as hosts for mistletoes may therefore facilitate the spread
Calvin, 2017; see also Table S1). In addition, the lack of host evidence
of mistletoes into new areas and habitats, where they can establish
may mask epiparasitic potential of other African mistletoes, such as
novel symbiotic interactions that impact local ecosystems.
Agelanthus kraussianus (detected on only two hosts; Table S1) and
probably some Viscum species (Wilson & Calvin, 2017).
3 | E PI PA R A S ITI S M A S A PAT TE R N O F
H OS T C H O I C E I N M I S TLE TO E S
Records of mistletoe autoparasitism in Africa, a peculiar type
of interaction in which a hyperparasite uses individuals of its own
species as hosts (Krasylenko et al., 2021), are found for only two
species—Globimetula braunii and G. cupulata (Table S1). Interestingly,
Epiparasitism as a type of plant hyperparasitism in which an aerial
these species apparently do not interact parasitically with any other
parasite (such as a mistletoe, love vine, or dodder) uses other para-
mistletoe, neither as epiparasites nor as hosts, suggesting their inter-
sitic plant as a host (Krasylenko et al., 2021), has been observed in
specific incompatibility. Of the other mistletoes occurring in Africa,
various parts of the world, most commonly in Oceania, but relatively
Viscum album is perhaps the one most known for its autoparasitic
few cases are known from Africa (Wilson & Calvin, 2017). Records
potential (Krasylenko et al., 2021), although the documented records
of 42 African mistletoe species from 10 genera acting as epipara-
come from that part of the species' range that lies outside Africa. As
sites show that this phenomenon is most common in Agelanthus,
it is difficult to distinguish autoparasitic individuals from their con-
Tapinanthus, and especially Viscum (Figure 3; Table S1). The latter
specific hosts, this interaction may be more common among mistle-
genus accounts for almost half of all epiparasite records on mistletoe
toes than reported (Krasylenko et al., 2021; Wilson & Calvin, 2017).
hosts in Africa and, together with Tapinanthus, harbors the great-
Importantly, autoparasitism should not be confused with the self-
est diversity of epiparasites. Among mistletoes, the most common
parasitism (i.e., attachment of haustoria to different parts of the
“epiparasite—parasitic host” combinations are Viscaceae epiparasitic
same individual plant), which is common in the mistletoes that form
1110
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KRASYLENKO Et AL.
epicortical roots and is sometimes referred to as epiparasitism, but is
feed on Helixanthera mannii in tropical regions (EOL, 2021). In South
a completely different phenomenon (Krasylenko et al., 2021; Wilson
Africa, elephants consume clumps of Moquiniella rubra, Viscum com-
& Calvin, 2017).
breticola, V. crassulae, and V. rotundifolium, despite these mistletoes
In addition, root hemiparasites (such as some Santalaceae) re-
usually reside on high branches (Midgley & Joubert, 1991). In turn,
portedly serve as common hosts for mistletoes in Asia and Australia
Thick-tailed Bushbaby (Otolemur crassicaudatus) was found consum-
(Wilson & Calvin, 2017), whereas the occurrence of this associ-
ing berries of Viscum songimveloensis (Oosthuizen & Balkwill, 2018).
ation in Africa has been greatly overlooked. African records asso-
African mistletoes attract also other mammals such as Bushveld
ciate epiparasitic mistletoes with three santalalean root-parasitic
Elephant-shrew
host genera: Olax (Olacaceae), Osyris (Santalaceae), and Ximenia
(Mastomys coucha), Natal Multimammate Mouse (M. natalensis),
(Elephantulus
(Ximeniaceae), which appear to be almost exclusively parasitized by
and Namaqua Rock Mouse (Aethomys namaquensis), which feed on
intufi),
Multimammate
Mouse
Loranthaceae (Figure 3). Ximenia seems to be the most susceptible
mistletoe fruits, especially during the winter season, when other
host, although this pattern may be biased by the relatively frequent
nutritional sources are scarce, and use habitats formed by mistletoe-
occurrence of Ximenia in habitats where the respective mistletoe
infected shrubs as shelter (Amutenya, 2017). Furthermore, the ev-
species occur, such as open woodlands and dry dense and gallery
ergreen mistletoe Tapinanthus bangwensis has been suggested as a
forests dominated by Combretaceae and Fabaceae species (Lompo
promising safe forage plant that does not cause digestive disorders
et al., 2021). Other Santalales have also been recorded as mistletoe
in ruminants and local poultry in Nigeria (Egbewande et al., 2011),
hosts in Africa, such as Diogoa, Heisteria, and Strombosia (Olacaceae)
and Ndagurwa and Dube (2013) reported that mistletoes are con-
(Table S1). Although the species of these genera are considered
sumed as highly nutritious supplements for goats.
autotrophic (Kuijt & Hansen, 2015), a more detailed study of their
Observations in the forests of Rwanda, the Democratic Republic
nutrient acquisition mechanisms may shed light on the functional
of the Congo and other areas of West Africa have shown that the
aspects of associated mistletoe parasitism.
leaves, fruits, and flowers of several mistletoe species (Agelanthus
Physiological ecology, evolutionary advantages, and ecosystem
brunneus, Englerina woodfordioides) are consumed by primates,
outcomes of epiparasitism in plants are poorly studied (reviewed
such as the Doggett's Blue Monkey (Cercopithecus mitis ssp. dog-
by Krasylenko et al., 2021), not to mention the remarkable cases
getti), the Tantalus Monkey (Cercopithecus aethiops), the Eastern
of tripartite associations such as the occurrence of Viscum verru-
Chimpanzee (Pan troglodytes schweinfurthii), and mountain gorillas
cosum on Tapinanthus quequensis on Agelanthus natalitius grow-
(Basabose, 2002; Kaplin et al., 1998; Weston, 2009). In Madagascar,
ing upon Combretum apiculatum (Combretaceae) in South Africa
the endemic Bakerella mistletoes serve as an important nutritional
(Nickrent, 2002). Limited evidence suggests that epiparasites tend
source for lemurs during the dry season (Irwin, 2008; Powzyk &
to sustain lower water potentials and higher concentrations of min-
Mowry, 2003). The sifakas (Propithecus diadema and P. edwardsi) rely
eral nutrients compared to parasitic and nonparasitic (primary) hosts,
on foliage, flowers, buds, and fruits of Bakerella clavata, especially in
likely leading to selection on associated herbivores (Krasylenko
fragmented forests due to the extended phenology of this mistletoe
et al., 2021). In addition, the tendency of epiparasites to have smaller
and its availability during the lean season, and despite its relatively
fruits and seeds compared with their parasitic hosts, as reported for
low protein content (Irwin et al., 2015; McGee & Vaughn, 2017).
some Viscaceae and Loranthaceae species from North America and
The same was assumed for cheirogaleid lemurs (Cheirogaleus
Africa (Calvin & Wilson, 2009), may affect the dispersal of epipar-
and Microcebus) in disturbed habitats (Atsalis, 2008; Crowley
asites by selecting for frugivores with certain dietary preferences.
et al., 2013). Similarly to Bakerella, Viscum ssp. may be a major food
source for Microcebus lemurs due to the high lipid content in fruits
4 | R EC I PRO C A L B E N E FIT S : M I S TLE TO E
FE E D E R S A N D P O LLI N ATO R S
compared to the loranths (Atsalis, 2008). Moreover, Bakerella ssp.
provide food resources for three birds and one bat species (Bollen
et al., 2004; Bollen & Van Elsacker, 2002).
The coevolution of mistletoes and birds has resulted in the ev-
In several biomes in Africa, including neighboring islands, mistletoes
ergreen clumps of semi-succulent foliage and attractive nutritious
are visited by mammals, birds, and insects for regular/concomitant
fruits being a valuable food source for many birds (Martínez del Rio
feeding. This type of feeding is most important in dry savannas and
et al., 1996). Raji et al. (2021) indicated 9 bird species that regularly
montane tropical forests, as these areas have high rates of mistletoe
forage on the fruits of Agelanthus dodoneifolius parasitizing Parkia
endemism and/or specialized intraspecific interaction between mis-
biglobosa and 71 species just visiting both the host trees and their as-
tletoes, their consumers, and hosts. Among mammals, nutrient-rich
sociated mistletoes in central Nigeria. The Stripe-cheeked Greenbul
mistletoe foliage is often preferred by ruminants in African drylands,
(Arizelocichla milanjensis) was observed feeding on Viscum shirense,
for example, in savannah (Ehleringer et al., 1986; Marshall et al., 1994).
Agelanthus subulatus, and Englerina inaequilatera fruits, while the
Large ungulates such as the Common Eland (Taurotragus oryx) and
Black-bellied Starling (Notopholia corrusca)—on Erianthemum ssp.
Greater Kudu (Tragelaphus strepsiceros) feed on mistletoe leaves in
(EOL, 2021). Moreover, Long-tailed Glossy Starling (Lamprotornis
the dry season (Roxburgh & Nicolson, 2008). In addition, various
caudatus), Blue-spotted Wood Dove (Turtur afer), and Speckled
species of Bovidae (antelopes, cattle, gazelles, goats, and sheeps)
Pigeon (Columba guinea) are considered as opportunistic mistletoe
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KRASYLENKO Et AL.
1111
feeders, but not their vectors (Boussim et al., 1993). Seven species
Apart from the Nectariniidae, some passerine birds such as the
of Nectariniidae observed on Phragmanthera dschallensis have been
White-eyes (Zosteropidae) are regarded as secondary pollinators,
identified as major nectar-feeders in East Africa (Gill & Wolf, 1975).
since they can open simpler flowers and forage nectar (Polhill, 1989).
Besides their trophic importance, mistletoes are known as important
Two species of White-eyes (Zosterops borbonicus and Z. chloronothos)
nesting and roosting sites for birds (Zuria et al., 2014). For instance,
endemic to Reunion and Mauritius, respectively, have been observed
the Gray Go-away-bird (Corythaixoides concolor, Musophagidae)
visiting the flowers of local Bakerella mistletoe species (Albert
nests in Plicosepalus kalachariensis and Viscum verrucosum in a semi-
et al., 2017; Gill, 1971). Of other birds endemic to Madagascar, the
arid savannah of southwest Zimbabwe (Ndagurwa et al., 2016).
Forest Fody (Foudia omiss, Ploceidae) and Velvet Asity (Philepitta
A variety of invertebrates interact with mistletoes during their life
castanea, Philepittidae) have also been observed as nectar feeders
cycle, using these plants as food and/or for reproduction in different
on Bakerella, and two species of Neodrepanis are known to suck
parts of the world (Burns et al., 2011; Zamora et al., 2020), although
nectar from the elongated flowers with their curved long beak
the relevant data from Africa are incredibly scarce and incoherent.
(Craig, 2014; Raherilalao & Goodman, 2011; Rakotomanana &
The one and most detailed community-level study in Africa was that
Rene de Roland, 2004). Feehan (1985), in his study on pollination
by Room (1971, 1972a, 1972b, 1973) on Tapinanthus bangwensis par-
mechanisms in African Loranthaceae, reported that nectar-feeding
asitizing cocoa (Theobroma cacao) in Ghanaian horticulture, which
birds are crucial for the pollination of Erianthemum mistletoes and
demonstrated the role of multipartite interaction networks (such as
that both size and shape of the pollinator's beak and its behavioral
“plant host – parasite – insect herbivore – predator”) in enhancing
patterns during flower visits define the pollination mechanism in
the impact of mistletoes on their host plants. More recently, the
Tapinanthus and Plicosepalus. In Cameroon, weavers (Ploceidae) with
effect of mistletoes on the arthropod abundance and diversity in
short thick beaks consume nectar of Tapinanthus flowers by piercing
the litter layer in a semi-arid savanna in southwest Zimbabwe has
the corolla tube without pollination, hence being nicknamed “nectar-
been assessed (Ndagurwa et al., 2014), and several other studies
robbers” (Kirkup, 1984; Weston, 2009).
addressed the diversity of Formicinae and Myrmicinae ants asso-
Apart from birds, some insects are known to be key pollinators
ciated with Phragmanthera capitata and P. nigritana in Cameroon
of some Viscaceae and Loranthaceae species (Godfree et al., 2003;
(Noutcheu et al., 2013; Ondoua et al., 2016). Numerous African mis-
Kuijt, 1969), although the records of such associations in Africa
tletoe species from different genera were recorded as hosts of cat-
are extremely rare. The genus Helixanthera, regarded as the most
erpillars of species of the Pieridae (Mylothris sp.) (Braby, 2005) and
primitive of the African Loranthaceae, might be the only one having
Lycaenidae (Iolaus sp. and Stugeta carpenteri) (Congdon et al., 2017).
flowers adapted to insect pollination (Dibong et al., 2008; Polhill &
Boussim et al. (1993) reported a small creamy-white butterfly forag-
Wiens, 1998). The honeybee (Apis mellifera) and a small social wasp
ing the flower tufts of Tapinanthus in Burkina Faso. The two above-
from the Vespinae visited the flowers of Agelanthus brunneus and
mentioned lepidopteran families, both of which have a cosmopolitan
A. djurensis in Nigeria, robbing nectar by making perforations in the
distribution, are known to contain many species whose larvae feed
bases of corollas (Weston, 2009; Weston et al., 2012).
exclusively on mistletoes (Watson et al., 2020).
The pollination of mistletoes occurs through abiotic (wind and
thermogenesis) and biotic components of ecosystems (Kuijt, 1969;
Mathiasen et al., 2008). Many tropical mistletoes have colorful flow-
5 | A E R I A L A N D TE R R E S TR I A L V EC TO R S
O F M I S TLE TO E S
ers producing large amounts of sugar-rich nectar that attract birds
and insects as pollinators (Mathiasen et al., 2008; Vidal-Russell &
Birds as crucial mistletoe dispersers, being either generalists or spe-
Nickrent, 2008). Although many mistletoes that are bird-pollinated
cialists with or without exclusive mistletoe feeding, are an impor-
are visited by a wide range of bird species, none of the latter can
tant component of the coevolving bird-mistletoe mutualistic system
be considered mistletoe specialists (Watson, 2001). In West Africa,
(Reid, 1991). Specialization of birds on mistletoe frugivory and dis-
mistletoe flowers are mainly pollinated by sunbirds (Nectariniidae),
persal has been well documented for Australia, South America, and
whose tapered and curved beaks with long mobile tongues are
tropical Asia as compared with Africa (Davidar, 1983; Martínez del
well-adapted to the morphology of the tubular flowers of the
Rio et al., 1996; Reid, 1989; Watson & Rawsthorne, 2013). At the
Loranthaceae, allowing for greater efficiency of flower visits. Species
same time, apart from their important contribution to long-distance
such as Western olive (Cyanomitra obscura), Green-headed (C. verti-
mistletoe dispersal and establishment of new patches (Watson &
calis), Scarlet-chested (Chalcomitra senegalensis), Northern double-
Rawsthorne, 2013), the ecological role of mistletoe generalists re-
collared (Cinnyris reichenowi), Variable (C. venustus), and Beautiful
mains unclear (Mellado & Zamora, 2014). This makes distinguish-
(C. pulchella) sunbirds are the most active in West Africa (Boussim
ing between generalist dispersers and fruit predators challenging,
et al., 1993; Raji et al., 2021; Weston et al., 2012). Olive-bellied
given the great diversity of frugivorous birds that feed on mistletoes
(Cinnyris chloropygius) and Collared (Hedydipna collaris) sunbirds have
(Mathiasen et al., 2008; Raji et al., 2021).
been specified as potential pollinators of Tapinanthus bagwensis in
The African Loranthaceae and Viscaceae produce bright-
Ghana (Room, 1972b), while Copper Sunbird (Cynnyris cupreus) – of
colored fruits, whose seeds are usually coated with sticky viscin
Agelanthus dodoneifolius in Nigeria (Raji et al., 2021).
(also called “birds' glue”) to attach firmly to a potential vector
1112
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KRASYLENKO Et AL.
(e.g., bird's feathers, beak, or legs) and to the host plant to en-
recognized as mistletoe vectors and defecated the seeds, favor-
sure establishment of the haustorium. Among the key aspects of
ing a much longer retention time in the birds' digestive tract and,
mistletoe dispersal is the ability of the vector to remove the fruit
hence, a much longer distance of dispersal (Godschalk, 1983c,
exocarp, being a precondition for breaking seed dormancy and
1985; Okubamichael, Rasheed, et al., 2011). Moreover, mousebirds
germination (Okubamichael, Rasheed, et al., 2011). Therefore, the
(Coliidae) and bulbuls (Pycnonotus) are considered long-distance dis-
role of vectors should only be assigned to those birds that have
persers because of their considerably long post-feeding flights and
been observed depositing mistletoe seeds on potential host trees,
great mobility during feeding (Godschalk, 1985; Green et al., 2009).
either in an aviary or in the wild (for an overview of avian vectors
The morphology of mistletoe fruits determines the range of avian
of African mistletoes, see Table S2). However, the related species
vectors, as seen in Viscum: the fruits with thick exocarps are dis-
(e.g., hornbills, turacos, mousebirds, and thrushes) that feed on
persed by tinkerbirds and barbets, while those with thin exocarps—
Viscum and Loranthaceae fruits, but for which there are no docu-
additionally by Knysna Turaco (Tauraco corythaix), bulbuls, and
mented records of seed deposition (Bosque et al., 2017; Brosset &
weavers (Godschalk, 1983a, 1983b).
Erard, 1986; Sun & Moermond, 1997) may also play a vector role,
so, this list is still incomplete.
It might be assumed that a highly specialized coevolutionary
plant-frugivore system, such as those involving mistletoe birds
Based on the way birds peel off the exocarp of mistletoe fruit
in Australia and flowerpeckers in Indo-Malaya, did not have
as a primary factor of vector efficiency, there are three approaches
enough time to have evolved in Africa, given a relatively recent
of bird's feeding on mistletoe fruits: regurgitation, defecation, and
(i.e., late Oligocene) origin of African Loranthaceae, forming the
bill wiping (Godschalk, 1985; Roxburgh, 2007). In an aviary exper-
youngest clade within the family (Liu et al., 2018). Tinkerbirds
iment with three bird species (Cape White-eye (Zosterops virens),
(Pogoniulus), regarded as specialists among avian vectors in the
Speckled Mousebirds (Colius striatus), and Red-winged Starling
forests and woodlands of central and southern Africa (Watson
(Onychognathus morio)) feeding on the fruits of Agelanthus natalitius,
& Rawsthorne, 2013), regurgitate the seeds as opposed to the
Okubamichael, Rasheed, et al. (2011) revealed that regurgitation
Australian and Asian mistletoe specialists which disperse the
provides the highest germination success, corroborating the findings
seeds via defecation (Polhill, 1989). The retention time of seed re-
of Roxburgh (2007) for Phragmanthera dschallensis.
gurgitation in an aviary was reported to be 10–15 min in the Red-
The distance of potential dispersal and type of avian vector feed-
winged Starling (Onychognathus morio) (Okubamichael, Rasheed,
ing, related to the time of gut passage or regurgitation of mistle-
et al., 2011) and ca. 20–24 min in the Black-collared Barbet (Lybius
toe seeds, are poorly studied. Some birds in the southern parts of
torquatus). The general speed of fruit removal is also very rapid in
Africa (e.g., Zambia and South Africa) contribute as short-distance
the Yellow-fronted Tinkerbird (P. chrysoconus) (Godschalk, 1985).
dispersers of mistletoe seeds between the same host species
This pattern of seed consumption and other behavioral features
within the existing mistletoe patches (Godschalk, 1985; Roxburgh
of tinkerbirds therefore restrict the long-distance dispersal of
& Nicolson, 2005).
African loranths despite their efficiency as vectors.
The main African mistletoe vectors are resident or mostly resi-
At the same time, the spread of Viscaceae seeds might also be
dent tinkerbirds (Pogoniulus). Thus, the breeding areas of Mustached
related to generalist avian feeders, for example, intra-African and
(P. leucomystax) and Yellow-rumped (P. bilineatus) Tinkerbirds in
Palearctic long-distance migrants. In their breeding areas in Europe,
Malawi forests are correlated with the presence of 4–6 mistletoe
some of them (e.g., Sylvia and Turdus) are recognized as frugivore
species (Dowsett-Lemaire, 1988; Polhill, 1989). A more widespread
vectors for many plants including mistletoes (Costa et al., 2014;
Yellow-fronted Tinkerbird (P. chrysoconus) visits mistletoe patches in
Mellado & Zamora, 2014). They may play an important role in the
its breeding territory and often infects the same host trees or the
long-distance dispersal of African mistletoes and the colonization
trees within individual patches due to regurgitating seeds soon after
of the new territories by patches, particularly in regions across the
their swallowing (Godschalk, 1985; Roxburgh & Nicolson, 2005,
Sahara, where mistletoes infect large numbers of hosts including in-
2008). This behavior potentially limits the likelihood that the bird
troduced and native ornamental crops (Dibong et al., 2008; Tizhe
will colonize new mistletoe patches and disperse the seeds at long
et al., 2016).
distances. A similar behavioral pattern has been observed in birds
The close mutualistic relationships between the Madagascan
with specialized digestive systems for rapid seed passage through
endemic Bakerella and its seed disperser, the Brown mouse Lemur
the gut—mistletoe birds (Dicaeum hirundinacum) in Australia and
(Microcebus rufus), are of particular interest. Bakerella seeds have
Phainopepla (Phainopepla nitens) in the New World (Reid, 1990;
been ingested and subsequently observed intact and sticky in the
Walsberg, 1975).
feces of lemurs on tree trunks (Atsalis, 2008). Due to the absence
However, data on the potential long-distance dispersal of mis-
of frugivorous birds on the island, small mammals such as some
tletoe seeds are missing. Using a theoretical vector-based model,
cheirogaleid lemurs may act as mistletoe short-distance vectors
Mokotjomela et al. (2013) estimated the potential seed dispersal
(Atsalis, 2008; Lahann, 2007). In addition, the Madagascar Flying Fox
distance for South African species—Cape White-eye (Zosterops cap-
(Pteropus rufus), also known to consume Bakerella fruits, is reputedly
ensis), Cape Bulbul (Pycnonotus capensis), and Speckled Mousebird
among the key long-distance seed dispersers on the island, espe-
(Colius striatus)—to be much greater than 8 km. These species were
cially in the isolated parts of fragmented forests (Bollen et al., 2004).
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KRASYLENKO Et AL.
6 | U N S E E N D I V E R S IT Y: E N D O PH Y TI C
A S S O C I ATE S O F M I S TLE TO E S A N D TH E I R
RO LE I N ECOS YS TE M S
1113
a disparity among endophytic assemblages in mistletoes suggests
non-random selection even among widespread fungal taxa without
host specificity. Though, this may also stem from undersampling
(Abreu et al., 2010) or the use of different techniques (cultivation-
The plant microbiome is an integrated functional unit comprising the
based and cultivation-independent) to assess endophytic community
exo- and endo-phytic microbiota (including bacteria, archaea, fungi,
patterns (Peršoh, 2013). Given that many associated saprotrophic
and protists) with their “theatre of activity,” whose roles in host plant
and wood-inhabiting taxa often dominate endophytic mycobiomes
life range from mutualism (e.g., promotion of plant growth and re-
in African non-parasitic woody plants that are known as mistletoe
sistance to various stresses) to neutral coexistence and to detrimen-
hosts (Begoude et al., 2010; Jami et al., 2015; Jordaan et al., 2006;
tal impacts on plant fitness and survival (Berg et al., 2020; Kalaiselvi
Linnakoski et al., 2012; Toghueo et al., 2017), detailed comparative
& Panneerselvam, 2021). The presence of a haustorium—the inter-
studies of endophytic assemblages in African mistletoes are needed
face between a mistletoe and its host plant—and the proximity of
to elucidate the patterns of their variation across the globe.
both associates within the same canopy make the mistletoe-host
The composition of mycobiomes in the surrounding environment
plant system an appropriate model for studying host preferences
and the host preferences of the fungi are thought to be the main
and specificity in bacterial and fungal endophytes. Nevertheless, the
factors determining the diversity and distribution patterns of mis-
mistletoe microbiome is just an emerging research topic, which is
tletoe endophytes (Peršoh, 2013). As suggested by studies both in
why the available information is scarce and pertains to few mistletoe
temperate and tropical ecosystems (Abreu et al., 2010; Guimarães
species analyzed to date.
et al., 2013; Hampel et al., 2016; Peršoh, 2013; Peršoh et al., 2010),
The microbiota of African mistletoes remains barely inves-
a mistletoe and its host plant would always exhibit an overlap in the
tigated, with only a few studies known to address the use of bio-
composition of their endophytic communities, although the degree
active compounds from a limited number of mistletoe-inhabiting
of this overlap is highly dependent on the geographic location and
ubiquitous fungi, such as Aspergillus, Penicillium, and Nigrospora
season. In addition, variation in plant organ selectivity and/or mode
(Abba et al., 2016; Ebada et al., 2016; Ladoh-Yemeda et al., 2015).
of transmission among endophytic fungi is also an important factor,
In addition, several older studies report a number of ascomycetes
as shown by the significant differences between mycobiomes asso-
(Asterinella, Clypeolina, Meliola loranthi, and a probable mycophile
ciated with different mistletoe organs (i.e., young vs. old leaves vs.
Septonema loranthi) and basidiomycetes (Aecidium cookeanum and
stems) (Abreu et al., 2010; Hampel et al., 2016; Peršoh, 2013). In
Septobasidium) associated with some mainland African Loranthaceae
view of the above evidence, mistletoes may play a role as a “bank”
1943;
of latent decomposers, pathogens, and other fungal guilds that are
Hughes, 2007). Balle (1964a) also reported A. cookeanum to infect
selected in mistletoe tissues (either by competition or differential
Socratina keraudreniana in Madagascar. In the temperate ecosystems
compatibility with the host) and then contribute to litter decomposi-
of Europe and North America, where this issue has gained more at-
tion and soil community function (Peršoh, 2013).
and
Viscum
species
(Balle,
1964a;
Hansford,
1937,
tention, mistletoes reportedly harbor taxonomically and functionally
Beneficial effects of endophytic fungi, including those of mis-
diverse endophytic communities dominated by ecologically pliable
tletoes, are also exhibited through the production of bioactive sec-
saprotrophic hyphomycetes (Capnodiales, Eurotiales, Hypocreales,
ondary metabolites, such as plant hormones, adenine ribosides,
Pleosporales), which are known to be common plant endophytes
flavonoid glycosides, as well as defense-related and aromatic com-
and litter decomposers (Hampel et al., 2016; Peršoh, 2013; Peršoh
pounds (Ebada et al., 2016; Pirttilä et al., 2004; Qian et al., 2014;
et al., 2010). Lower occurrence was reported for wood-decaying and
Tanaka et al., 2005; Tudzynski, 1997). Thus, endophytes are in-
corticioid fungi (e.g., some Coniochaetales and Xylariales) and yeasts
volved in processes related to important plant functional traits,
(Saccharomycetales and Tremellales from Europe), with sporadic
including the resistance to pathogenic organisms and synthesis of
occurrences of ectomycorrhizal (in Europe) and mycophilous taxa.
plant volatiles. For instance, the ability to suppress plant patho-
Many of these fungi are known opportunistic plant pathogens (e.g.,
gens has been demonstrated for some American and African mis-
Alternaria, Colletotrichum), and several mistletoe-specific species
tletoe endophytes (Abba et al., 2016; Martin et al., 2012; Ribeiro
have also been recorded (Baranyay, 1966; Karadžić & Lazarov, 2005;
et al., 2018), whereas an endophytic ascomycete Lasiodiplodia
Kotan et al., 2013; Shamoun et al., 2003; Wicker & Shaw, 1968).
produced essential floral oil components in Viscum coloratum from
Reports from tropical South America indicate—as major differ-
East Asia (Qian et al., 2014). Plant volatiles provide cues to next-
ences from the above patterns—the apparent rarity of taxa that
level consumers such as insect herbivores, parasitoids, and pol-
are otherwise common plant endophytes in the tropics (e.g., some
linators (Ponzio et al., 2013; Schiestl, 2015). The latter, in turn,
Botryosphaeriales, Glomerellaceae, and Xylariaceae), and the high
play a role in the transfer of bacteria and microfungi between
frequency of the ubiquitous Diaporthaceae (such as Phomopsis),
and within plants, contributing to the spatiotemporal turnover
which have not been recorded as associates of temperate mistle-
of the microbiotas between plant vegetative organs, floral parts,
toes. This is coupled with the lack of records of the guilds that occur
nectar and pollen, and seeds, which then transfer these microbes
as incidental symbionts in temperate mistletoes, such as yeasts and
(along with those acquired internally) to the next plant genera-
mycorrhizal fungi (Abreu et al., 2010; Guimarães et al., 2013). Such
tion (Álvarez-Pérez & Herrera, 2013; Goelen et al., 2020; Prado
1114
|
KRASYLENKO Et AL.
et al., 2020). Mistletoes raise the complexity of these multitrophic
route for the unwanted intrusion of mistletoes into new areas and
interactions, involving plant endophytes, to a new level by blend-
natural habitats where they may spread in an uncontrollable manner
ing (both internally and externally) into the symbiont communities
due to the lack of specific consumers or other limiting factors. Crops
of their host plants to form shared symbiotic networks with addi-
planted in large quantities and visited by generalist pollinators and
tional trophic links.
frugivores (Bennett et al., 2021) may therefore facilitate the spread
of mistletoes across the continent. It is thus essential to unravel the
7 | CO N C LU S I O N S A N D FU T U R E
PE R S PEC TI V E S
feeding habits, population dynamics, migration routes, and mistletoe
dispersal efficiency of frugivores recorded as potential or recognized
mistletoe vectors. This would provide a rich source of information to
improve our knowledge on mistletoe biogeography and current dis-
Mistletoes, as important components of the African flora, attract
tribution patterns in Africa, as well as guide crop industries and en-
great interest from researchers all over the world due to their
vironmental planning programmes in managing their plant resources
peculiar evolution, extensive network of biotic interactions, and
to restrain the spatial distribution of mistletoes by seed dispersers
unique pollination and seed dispersal strategies. Nevertheless,
(Griebel et al., 2017).
there are significant knowledge gaps in many aspects of African
In addition, the use of plant pathogens (such as fungi and bac-
mistletoe ecology, highlighting the need for multidisciplinary and
teria) in biological control of pest mistletoes is increasingly gaining
field-based studies that address both fundamental (e.g., evolu-
attention as an environmentally beneficial method applicable to
tionary and biogeographic reconstructions, taxonomic updating,
agroecosystems (Shamoun et al., 2003). Given the potential success
physiology and ecology of multitrophic interactions, and ecosys-
and major challenges of this method as outlined by the recent ef-
tem impacts) and applied aspects at pan-African and local levels.
forts of its implementation against Viscum album in Europe (Kotan
Among the latter, the use of mistletoes for the production of bio-
et al., 2013; Poczai et al., 2015; Varga et al., 2014), designing targeted
active compounds with multiple applications (e.g., in biocontrol of
studies on the identification and use of specific mistletoe pathogens
agricultural pests) is a promising challenge that deserves atten-
in Africa would be crucial for controlling mistletoes in areas where
tion. In addition, more attention should be given to issues related
they threaten crop production.
to the conservation of declining mistletoe species, which play a
key role in wildlife communities.
AU T H O R C O N T R I B U T I O N S
Disentangling the interactions within symbiotic communities
YK involved in conceptualization, data curation, funding acquisi-
associated with mistletoes is key to understanding the role of
tion, investigation, methodology, supervision, validation, visualiza-
these plants in ecosystems. Many aspects of such interactions,
tion, and writing—original draft, review and editing. TRK involved in
including those between organisms of different phyla and with
conceptualization, funding acquisition, investigation, and writing—
contrasting life histories, have so far been studied in non-parasitic
original draft, review and editing. YS involved in conceptualization,
plants and without considering the possible bottom-up effects
data curation, formal analysis, investigation, validation, visualization,
(such as nutrient and metabolite exchange, cross-talks with co-
and writing—original draft, review and editing. NA involved in con-
existing organismic communities). Little-studied associations
ceptualization, data curation, investigation, validation, visualization,
that are particularly interesting when applied to the mistletoe-
and writing—original draft, review and editing. KHT involved in con-
host plant system include the reciprocal relationships between
ceptualization, investigation, and writing—original draft, review and
plant visitation by different insect guilds and the composition of
editing. OH and GR involved in investigation and writing—review
phyllosphere-associated microbial communities (Bitar et al., 2021;
and editing.
Goelen et al., 2020), or the effects of nectar microbiota on plant
pollination success (Rering et al., 2020). The perennial above-
AC K N OW L E D G M E N T S
ground growth habit and easily traced physical contact with the
We thank the fine artist Natalia Pendiur (Kyiv, Ukraine) for the graph-
host in mistletoes (in contrast to the root-hemiparasites) make
ical drawing of Figure 1. Luiza Teixeira-Costa (Harvard University
them a perfect model for studying functional links within and
Herbaria, Cambridge, USA) is greatly appreciated for the profes-
between different trophic levels to reveal interlevel nutrient and
sional consultation regarding the haustorial types in African mistle-
energy flux pathways, patterns of horizontal gene transfer, and
toes. This study was partially supported by the European Regional
large-scale trends in ecosystem functioning.
Development Fund (ERDF) project “Plants as a tool for sustainable
It is widely acknowledged that mistletoes can make detrimental
global development” (grant No. CZ.02.1.01/0.0/0.0/16_019/000
impacts on parasitized woody crops, affecting the fitness, yield, and
0827 to YK). The Alexander von Humboldt foundation sponsored
longevity of host plants (Dibong et al., 2008). Of particular concern
TRK by providing useful materials. Private joint stock company (PJS)
is the fact that many economically important plant species, including
“Carlsberg Ukraine” (Kyiv, Ukraine) supported authors’ studies in
both native and introduced ones, are susceptible hosts for numerous
frames of the development of the unmanned aerial vehicle called
mistletoe species in Africa. Planted across the continent and serving
“Druid Drone” for mistletoe observation and sample collection.
as a reservoir for mistletoe germplasm, these crops provide a living
Open Access funding enabled and organized by Projekt DEAL.
|
KRASYLENKO Et AL.
C O N FL I C T O F I N T E R E S T
The corresponding author confirms on behalf of all authors that
there have been no involvements that might raise the question of
bias in the work reported or in the conclusions, implications, or opinions stated.
DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are openly available in the Open Science Framework repository (10.17605/OSF.IO/
KVZYM), as well as in the Supporting Information.
ORCID
Yuliya Krasylenko
https://orcid.org/0000-0001-7349-2999
Tonjock Rosemary Kinge
https://orcid.
org/0000-0002-5402-1021
Yevhen Sosnovsky
Natalia Atamas
https://orcid.org/0000-0003-0391-3502
https://orcid.org/0000-0002-1072-8826
Katamssadan Haman Tofel
https://orcid.
org/0000-0003-1791-3888
Oleksii Horielov
Gerhard Rambold
https://orcid.org/0000-0003-3970-9570
https://orcid.org/0000-0002-9473-3250
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S U P P O R T I N G I N FO R M AT I O N
Additional supporting information can be found online in the
Supporting Information section at the end of this article.
How to cite this article: Krasylenko, Y., Kinge, T. R., Sosnovsky,
Y., Atamas, N., Tofel, K. H., Horielov, O., & Rambold, G. (2022).
Consuming and consumed: Biotic interactions of African
mistletoes across different trophic levels. Biotropica, 54,
1103–1119. https://doi.org/10.1111/btp.13130