Review
Host specificity in parasitic plants—perspectives
from mistletoes
Desale Y. Okubamichael*1,2, Megan E. Griffiths1,3 and David Ward1,3
1
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, 3209, South Africa
Plant Conservation Unit, Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch, 7701,
South Africa
3
Department of Biological Sciences, Kent State University, Kent, OH 44242, USA
2
Received: 20 June 2016; Accepted: 14 September 2016; Published: 22 September 2016
Associate Editor: W. Scott Armbruster
Citation: Okubamichael DY, Griffiths ME, Ward D. 2016. Host specificity in parasitic plants—perspectives from mistletoes.
AoB PLANTS 8: plw069; doi: 10.1093/aobpla/plw069
Abstract. Host specificity has been investigated for centuries in mistletoes, viruses, insects, parasitoids, lice and
flukes, yet it is poorly understood. Reviewing the numerous studies on mistletoe host specificity may contribute to
our understanding of these plants and put into context the dynamics at work in root parasitic plants and animal
parasites. The mechanisms that determine host specificity in mistletoes are not as well documented and understood
as those in other groups of parasites. To rectify this, we synthesized the available literature and analyzed data compiled from herbaria, published monographs and our own field studies in South Africa. As for other groups of parasites, multiple factors influence mistletoe host specificity. Initially, pollination affects gene flow. Subsequently, seed
dispersal vectors (birds and marsupials), host abundance and compatibility (genetic, morphological, physiological
and chemical), history and environmental conditions affect the interaction of mistletoes and their hosts and determine host specificity. Mistletoe–host network analyses and a geographic mosaic approach combined with long-term
monitoring of reciprocal transplant experiments, genetic analyses of confined mistletoe populations and comparative phylogenetic studies could provide further insights to our understanding of host specificity. Some of these
approaches have been used to study animal–plant interactions and could be adopted to test and evaluate host specificity in mistletoes at local and larger geographic scales.
Keywords:
Bird dispersal; coevolution; geographic mosaic; haustorium; host compatibility; parasitic plants.
Introduction
Parasitic plants are very diverse (3500–4000 species)
and display a considerable variation in host-specificity
(Norton and Carpenter 1998; Norton and de Lange 1999;
Thorgood and Hiscock 2010). However, our understanding
of the evolution, ecology and speciation of host-specific
parasitic plants remains limited (Ntoukakis and Gimenze-
Ibanez 2016). Aerial parasitic plants—commonly called
mistletoes, a term that describes a polyphyletic group of
organisms with similar life histories—have also received
little research attention because they generally cause less
damage to commercial plants compared to root parasites
(Yoder 1999; Mathiasen et al. 2008; Ntoukakis and
Gimenze-Ibanez 2016). Yet, they provide an opportunity to
* Corresponding author’s e-mail address: dessu81@gmail.com
C The Authors 2016. Published by Oxford University Press on behalf of the Annals of Botany Company.
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explore the origins of host specificity as a prerequisite for
speciation in parasites. There are also substantial
studies on mistletoe host specificity that can inform the
broader study of plant and animal parasites. To link
mistletoe studies with root parasitic plants and animal
host specificity, a comprehensive review of our current understanding of host specificity in mistletoes is
required.
Mistletoes are obligate hemiparasites that depend on
hosts for water and nutrients and vary in their host use
preference or specificity (Calder and Bernhardt 1983;
Press and Graves 1995). Host specificity is the restricted
use of available potential host species at a local scale,
while host preference refers to the hierarchical ranking
of host use (Thompson 1988; Norton and Carpenter
1998). For the purpose of this review, we view preference
by mistletoes for particular hosts as a form of host specificity. In Africa, 70 % of mistletoes are generalist species
that parasitize hosts from several families, 12 % are specific on hosts from one family but occasionally parasitize
a few genera of other families and 18 % are specific to
one or a few host species of a single genus (Polhill and
Wiens 1998). The generalist mistletoes may encounter
host species that vary in compatibility at different locality, thus may parasitize a subset of available host species
at a given locality. This process could drive mistletoe specialization by selecting for host-specific adaptation at a
local level (Norton and Carpenter 1998; Norton and de
Lange 1999; Amico et al. 2007; Blick et al. 2012;
Kavanagh and Burns 2012).
Mistletoes that are initially capable of utilizing several
host species may also become restricted to a subset of
available hosts within an area (Barlow and Wiens 1977;
Amico et al. 2007; Okubamichael et al. 2011a; Kavanagh
and Burns 2012, Lira-Noriega et al. 2015; Lira-Noriega
and Peterson 2014). Generalist mistletoe species are
therefore often composed of distinct host-specific populations (e.g. Lira-Noriega et al. 2015; Lira-Noriega and
Peterson 2014). These host-specific populations of
mistletoes could eventually speciate to produce host
races (Norton and de Lange 1999; Jerome and Ford
2002; Lira-Noriega et al. 2015). Several factors such as
seed dispersal vectors, host availability, host abundance,
host compatibility and suitable niche for the parasite determine host specificity in mistletoes.
While a geographic mosaic approach is used widely to
explain the relationship between specialization and
coevolution, particularly within host–parasite associations in animals (sensu Thompson 1988, 1989, 1993,
1994, 1997, 2005a, b), it is rarely applied to mistletoe–
host interactions. In this review, we propose a geographic mosaic approach that may help to explain
mistletoe host specificity and at the end we suggest this
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to be integrated with the current understanding of host
specificity.
Mechanisms That Determine
Host Specificity
Pollination by diverse mechanisms and seed dispersal
mainly by birds initially affects the gene flow and the distribution of mistletoes on host trees. Thereafter, diverse
host traits influence the establishment and survival of
mistletoes, further filtering the distribution of mistletoes
among host trees. Pollination of mistletoes is carried out
by insects, birds and, rarely, by wind (Kirkup 1998; Tadey
and Aizen 2001; Watson 2001). Thus, several different
animal agents act as potential visitors to potential host
trees. Self-compatibility in mistletoes is known to limit
outcrossing and enhance inbreeding with nearby individuals (Vaknin et al. 1996; Ladley et al. 1997). In addition,
differential flowering times among mistletoes may deter
gene flow among species even in the same locality. For
example, Amico et al. (2007) reported that peak flowering times of Tristerix aphyllus and the sympatric T. corymbosus do not overlap greatly, which limits interspecific
pollen transfer. This is one of the factors believed to have
influenced speciation in these two species in the genus
Tristerix. Arceuthobium americanum, an obligate outcrossing species, also has limited pollen dispersal (maximum 400–512 m) and increases population
differentiation (Jerome and Ford 2002). Preferential pollen transfer among individuals growing on the same or
nearby trees may limit pollen flow among host races as
well. Most importantly, natural hybridization of mistletoes is very rare and the success of a hybrid seedling
would require an intermediate host that is unlikely to
exist (e.g. Amyema pendulum and A. quandang produced
only first-generation hybrids) (Bernhardt and Calder
1981; Calder et al. 1982). Natural hybridization is also almost absent in New World Arceuthobium (Hawksworth
and Wiens 1996). Therefore, pollination acts as an important isolating mechanism for sympatric mistletoes.
Mistletoe species often rely on birds for direct seed dispersal (Aukema 2003). Only the dwarf mistletoes
(Arceuthobium spp.) have seeds that are dispersed explosively (Hawksworth and Wiens 1996; Kelly et al.
2009), while Misodendrum is dispersed by wind (VidalRussell and Nickrent 2007) and Tristerix by marsupials
(Amico and Aizen 2000). In bird-dispersed mistletoe species, the birds consume mistletoe fruits and subsequently wipe their bills, regurgitate or defaecate the
seeds on the branches of host trees (Reid 1991; Aukema
2003; Roxburgh 2007; Green et al. 2009; Okubamichael
et al. 2011b). Birds break the physical dormancy of the
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seed and initiate germination by removing the fruit cover
(exocarp), which otherwise inhibits germination
(Roxburgh 2007; Okubamichael et al. 2011b). The behaviours of the birds also expose the sticky viscin, enabling
the mistletoe seeds to firmly attach to branches of host
trees. Mistletoes and their dispersers have reciprocally
evolved, although the nature of this coevolution is diffuse (see Reid 1991 and references therein). Some
mistletoe species have developed contrasting colours of
red, black, purple and dark blue that target specific frugivorous birds (Reid 1991). In turn, the avian genus
Dicaeum (mistletoe birds) have modified tongues and
crops that allow them to efficiently process mistletoe
fruits (Reid 1991). They also frequently disperse the
seeds to suitable host branches where the mistletoes
can establish (Reid 1991). Similarly, members of the bird
genus Phainopepla have a specialized digestive system
and breed during the fruiting season of the desert mistletoes (Phoradendron californicum) (Walsberg 1975).
Bird dispersers determine the frequency of interaction
of mistletoes with their hosts through the dispersal of
their seeds to the host trees, and by determining the specific location of where seeds are placed on trees, which is
key to mistletoe survival (Carlo and Aukema 2005). Birds
usually disperse more mistletoe seeds on the parental
host tree than elsewhere (Aukema and Martınez del Rio
2002a, b; Aukema 2003; Carlo and Aukema 2005). As
with many other plant species, there is a negative correlation between mistletoe seed survival and dispersal distance from the parent plant (Okubamichael et al. 2011b).
Birds are responsible for the local aggregation of mistletoes at a locality (infestation patches) or on individual
trees (infection intensity) and determine a negative binomial distribution of mistletoes at the population level
(Overton 1994; Robinson and Geils 2006). Marsupials like
the Colocolo Opossum (Dromiciops gliroides) also had
similar effects on aggregation in mistletoe (T.corybosus)
infection that matched to their abundance in space in
the temperate forests of Patagonia (Garcıa et al. 2009).
Dispersal by animal vectors determines mistletoe–
host interactions across time and space, which in turn influences the geographic mosaic of mistletoes and their
hosts. Birds are able to transfer mistletoe seeds across
large distances and potentially disperse seeds to very
distantly related hosts as well (Aukema and Martınez del
Rio 2002a, b). Birds also potentially facilitate host
switches by depositing mistletoe seeds on hosts that are
not preferred. For example, in T. aphyllus and T. corymbosus, it is postulated that T. aphyllus arose from ancestral
T. corymbosus seeds being deposited on a rare cactus
host by mockingbirds that prefer high perches. Over
time, some of these seeds became established and
eventually developed reproductive isolation from
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T. corymbosus (Amico et al. 2007). Birds may also enhance the interactions between mistletoes and their prospective hosts, for instance, if the host trees provide a
reward such as fleshy fruits that are available at the
same time as the mistletoe fruits (Carlo and Aukema
2005; Okubamichael et al. 2011b). In either case, birds
may potentially influence host specificity and host
switches in mistletoes.
Birds may learn through time to differentially visit certain host species based on the reward of mistletoe fruits
found only on infected trees (Godschalk 1983, 1985). The
reward being offered increases the chance of efficient
dispersal of mistletoe seeds to the appropriate host
thereby facilitating host specificity (Martınez del Rio et al.
1995; Aukema and Martınez del Rio 2002a). Host specificity also enhances aggregation of individual mistletoes
on trees of the specific host, which ensures that birds
preferentially and constantly visit the same mistletoes
and makes pollination frequent and easy (Watson 2011).
In this regard, mistletoe species with high host specificity
could be selected over those that are host generalists.
Future research should investigate seed dispersal strategies of host generalist and specialist mistletoes by
investigating fruit traits such as size, colour and nutritional quality. Specialist mistletoes would be expected to
have fruit traits that target specific birds capable of directing seed dispersal to the appropriate host, thereby
increasing fitness of the mistletoe species.
Host Abundance and Compatibility
Diverse factors, but especially host traits, influence the
establishment and survival of mistletoes and these traits
further affect the distribution of mistletoes among host
trees. In plant communities where species diversity is
high and there are few dominant species, such as in rain
forests, mistletoes tend to be generalists (Barlow and
Wiens 1977). High host specificity is not likely to confer
any selective advantage in such environments. Instead,
there may be selection for traits that allow the mistletoes to infect and grow on a wide range of host species
(Press and Graves 1995; Downey 1998). This clearly indicates that host abundance is an important trait that influences mistletoe host specificity. In less diverse
temperate forests and semiarid savannas, where dominance of one or a few tree species is typical, mistletoes
are more likely to be specific to one genus or even to a
single host species (Norton and Carpenter 1998;
Okubamichael et al., 2011a). In these environments selection favours close physiological adaptations of the
mistletoes to the predominant host species (Barlow and
Wiens 1977; Dean et al. 1994; Downey et al. 1997;
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Downey 1998). There are many long-term associations
of hosts and mistletoes that have evolved in a restricted,
unidirectional way and that have resulted in extremely
host-specific mistletoes (Norton and Carpenter 1998;
Barlow and Wiens 1977). However, there are also instances where mistletoes parasitize uncommon host
trees as a result of host compatibility at the genetic,
mechanical, physiological and biochemical level (Yan
1993a; Yan and Reid 1995; Okubamichael et al. 2011a;
Fadini 2011). This may create a geographic mosaic of
mistletoe–host combinations across the landscape.
Usually the ever-changing composition of plant communities creates opportunities for new interactions between the mistletoe and host species (Thompson 1999).
Thus, specialization may be a dynamic state capable of
changing rather than being a static endpoint. Mistletoes
have shorter generation times and higher reproductive
rates than their host trees, which enable them to adapt
quickly to a shift in host abundance in the ecosystem
(Norton and Carpenter 1998). The shorter life cycle of the
mistletoes may also facilitate a more rapid adaptation to
host genotypes than the emergence of new resistance
by host genotypes. When hosts develop resistance, selection would favour traits in the mistletoe that increase
virulence or otherwise allow them to overcome host resistance or undergo host switching. This is largely consistent with the Red Queen Hypothesis or the evolution
of an ‘arms race’ (van Valen 1973; 1976; Jokela et al.
2000; de Vienne et al. 2012). Specific research on this
topic in mistletoes is lacking, and it would enhance our
understanding of parasitism evolution in mistletoe.
The evolution of haustoria has enabled parasitic plants
to acquire water and nutrients from other plants. It is
suggested that parasitism in plants has evolved in arid
environments where water and nutrients are limited
(Atsatt 1973, 1977; Ehleringer et al. 1985; Bowie and
Ward 2004). Nitrogen is often a limiting nutrient in
plants, and mistletoes have been hypothesized to selectively parasitize host species that are high in nitrogen
(Ehleringer et al. 1985; Midgley and Joubert 1991; Dean
et al. 1994; Pennings and Callaway 2002). For example,
Dean et al. (1994) found that mistletoe species richness
was positively correlated with the average nitrogen level
of the plant community in major vegetation types in
South Africa. However, Griffiths et al. (2016) used a
phylogenetically independent analysis of the Dean et al.
(1994) data and found that the area occupied by a host
species was more important than nitrogen in determining mistletoe species richness. This suggests that the
quality of host trees in terms of nitrogen content may
not be as critical as previously thought in terms of driving
host specificity in mistletoes. This was even more pronounced in a global study by Scalon and Wright (2015)
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that showed nitrogen is not the limiting nutrient for
mistletoes.
In any parasite–host association a parasite evolves
traits that aid in effectively getting into the host. In response, the hosts usually build resistance to parasite infection (Thompson 1994, 2005a; Medel et al. 2010).
Although in animals the relationship between immunology and resistance and susceptibility is known, comparable knowledge on parasitic plants and their host
associations is absent. In mistletoes, the haustorium
may encounter a range of resistance pressures by potential host trees, in which some individuals or host species
are susceptible and some are resistant at various phases
of haustorium penetration. The bark of many non-host
plant species is resistant to haustorial penetration by
mistletoes (Yan 1993a). Mistletoe infection could,
through this process, be blocked before establishment
can occur. For example, non-host species sometimes develop a wound periderm that blocks access to the xylem,
thereby curtailing further establishment of mistletoes
(Yan 1993a). Yan (1993a) showed that the primary host
species of the mistletoes studied showed an initial bark
resistance, which may be an important evolutionary
adaptation to reduce infection. However, none of the primary host species exhibited xylem resistance. Thus, host
trees may reject infection at different stages of mistletoe
establishment by thwarting mistletoe penetration or
blocking access to water and nutrients. There is also a
suggestion (Hawksworth and Wiens 1996) that host
trees could block the flow of xylem or phloem to infected
branches, which obviously causes the death of the
branch but protects the whole individual from nutrient
drain to the parasite.
It is plausible to suggest that mistletoes could coadapt with their hosts in the short-term and in the longterm and could co-speciate and shift hosts, but there are
limited data to support this proposal. For example, Medel
et al. (2010) recorded two cactus species (Echinopsis chiloensis and Eulychnia acida) having extremely long
spines that deter infection by the mistletoe T. aphyllus.
Mistletoe-dispersing Chilean mockingbirds (Mimus
thenca) avoid perching on certain cactus hosts
(Echinopsis chiloensis and Eulychnia acida) with extremely long spines (Martınez del Rio et al. 1995). Hence,
host individuals with longer spines have lower mistletoe
infection rates than those with shorter spines (Martınez
del Rio et al. 1995). Even if birds disperse mistletoe seeds
to long-spined cacti, the seeds remain hanging on the
spine and their hypocotyl dies before it can form a holdfast on the host. In response, the mistletoes (T. aphyllus)
have evolved a very long hypocotyl (the structure that
protrudes as the mistletoe germinates and attaches to a
host twig before forming a haustorium) that parasitize
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long-spined cactus hosts (Medel et al. 2010).
However, such reports are rare in the literature on
mistletoe–host coevolution. Therefore, host specificity
can be used as a potential measure of coevolution
(Thompson 1989).
At an early germination stage, mistletoe seeds are
known for site- and host-insensitive nature, i.e. germinate quickly and indiscriminately on any substrate
(Glazner et al. 1988; Yan 1993b; Rödl and Ward 2002).
After germination, mistletoe survival depends on the
successful attachment and penetration to the vascular
tissue of the host tree. There is considerable evidence
that mistletoe performance on different host trees
varies. Clay et al. (1985) found that development of haustorial disks of Phoradendron tomentosum seedlings was
significantly greater when experimental host and source
host species were the same, rather than different, species. Okubamichael et al. (2014) also obtained a similar
result demonstrating that hypocotyls of Agelanthus
natalitius seedlings grew longer within their own source
hosts. Dodder (Cuscuta pentagona), an aerial parasite,
but not a mistletoe, also uses volatile chemicals released
by the host to sense the location of the hosts and to cue
haustorium development on preferred host species
(Runyon et al. 2006). As yet there is not sufficient evidence on the role of volatile compounds and bark chemistry in directing host specificity in mistletoes. Even
though the specific chemical interactions for mistletoes
and their hosts are not known, many root parasites may
require chemicals or a contact signal to recognize a host
and initiate the development of the haustorium (haustorium-inducing factors (HIF), the flavonoids xenognosin A and B, quinone 2,6-dimethoxy-1,4-benzoquinone)
(Jamison and Yoder 2001; Westwood et al. 2010) or they
require a host chemical signal for germination
(Strigolactones) (Xie et al. 2010; Ćavar et al. 2015).
Tomilov et al. (2006) indicated that HIFs might be species
specific and activate specific receptors in particular parasites or host plants that may produce several HIFs with
possible redundancy of active molecules.
Geographic Mosaic Approach
Coevolution is a reciprocal evolutionary change in interacting species at local, regional and global levels that is
driven by natural selection, creating ever-changing geographic mosaics of species interactions with one another
(Thompson 1989, 1994, 2005b). Thompson (2005b)
argues that the coevolution between pairs of species or
populations within a local scale must be maintained to
eventually establish the interaction across a broader
geographic range. Thompson (1997, 2005b) describes
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this as a geographic mosaic model and proposes that
coevolving interactions, which collectively drive ongoing
coevolutionary dynamics of global biodiversity, incorporate three components: geographic selection mosaics,
coevolutionary hotspots and trait remixing.
Genotype-by-environment interactions determine the
fitness of interacting species across regions. Natural selection acts on this variation causing population specialization in different regions, which is referred to as
geographic selection mosaics. Coevolutionary hotspots
are subsets of communities in which much of the evolutionary change occurs where local selection is nonreciprocal. Such coevolutionary hotspots are also often
embedded in a broader matrix of coevolutionary coldspots (Gomulkiewicz et al. 2000). The geographic range
of a parasitic species may only overlap with that of its
preferred host(s) at certain localities. The three-way
interaction between mistletoe–bird–host (Reid 1991;
Aukema and Martınez del Rio 2002a, b) may create
coevolutionary hotspots in which certain local populations contribute greatly to the overall coevolution between the mistletoes and their hosts. This could create a
mosaic of mistletoe–host association, which varies
through space and time. Trait remixing occurs through
changes in the genetic structure of coevolving species
due to mutations, gene flow, random genetic drift and
extinction of local populations. The continuous altering
of the spatial distributions of potentially coevolving
genes and traits often drives the processes of coevolution (Thompson 2005b).
The works of Lira-Noriega et al. (2015) and LiraNoriega and Peterson (2014) on the mistletoe
Phoradendron californicum have demonstrated that the
distribution of this species is strongly affected by the
evolutionary hot spots where the host, dispersal vectors
and environmental condition of the mistletoes overlap.
Their studies highlight the importance of the geological
past interacting with the mistletoe–host associations in
structuring phylogeography and initiating host races in
mistletoes. Using herbarium voucher specimens,
Lira-Noriega and Peterson (2014) tested three niche
hypotheses (host, vector and parasite) that likely mediate mistletoe distribution and found that host availability
alone does not determine mistletoe establishment.
Instead, suitable environmental conditions for the
mistletoe are a prerequisite. Jerome and Ford (2002)
showed that Arceuthobium americanum has at least
three distinct genetic host races that potentially could
undergo speciation with time. Most importantly, these
studies clearly demonstrate that a geographic mosaic
approach can explain the mosaic nature of the distribution of mistletoes and patterns in host specificity.
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Host Specificity in South Africa from
Literature, Herbaria and Field
Observations
It is important to investigate host specificity at the family, genus and species levels because the available species that can be parasitized at particular levels vary, and
not all species in a genus can be parasitized equivalently
by specialist mistletoes. Unfortunately, monographs for
mistletoes in Africa only report host use mainly at the
genus level (Polhill and Wiens 1998; Wiens and Tolken
1979; Visser 1981). Analyses of Shannon-Wiener indices
(H’) of data from the mistletoe literature (Polhill and
Wiens 1998; Wiens and Tolken 1979; Visser 1981) show
that the two main mistletoe families in southern Africa
parasitize a high diversity of host genera. Mistletoes from
Loranthaceae parasitize 89 host genera with H’ ¼ 4.26,
while those in Viscaceae parasitize 65 host genera with
H’ ¼ 4.05 (Fig. 1). Many of the southern African mistletoes in these two families use Acacia and Combretum as
Figure 1. The number of parasitized host genera by the prospective mistletoe species (data modified from Visser, 1981). This summarizes the pattern of infection of the common mistletoe species
found in southern Africa of the two largest families of mistletoes:
(A) Loranthaceae and (B) Viscaceae.
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their main host plants. A few mistletoe species are very
host-specific and use only one genus over their entire
geographic range (e.g. Viscum minimum parasitizes only
Euphorbia horrida and E. polygona in the Eastern Cape,
South Africa) (Polhill and Wiens 1998).
Using specimens from the Bews Herbarium at the
University of KwaZulu-Natal, we compiled data to give us
a more comprehensive understanding of host use by
mistletoes that can be traced to the species level [see
Supporting Information—Appendix 1]. The collection
includes 340 herbarium specimens of mistletoes from
Loranthaceae (46 mistletoe species recorded from over
200 host species), and 179 herbarium specimens of
mistletoes from Viscaceae (14 mistletoe species recorded from over 70 host species). From the herbarium
investigation it is clear that Acacia karroo and A. caffra
were the most commonly used host species in South
Africa (Fig. 2). This may be related to the availability of
these Acacia species, as A. karroo is the most widely distributed Acacia species in South Africa (van Wyk and van
Wyk 1997). However, in areas where A. karroo is not the
most abundant potential host species, many mistletoe
species are found on other host species (Fig. 2). Viscum
rotundifolium was found parasitizing the highest number
of host species in KwaZulu-Natal, but it was restricted to
Ziziphus mucronata in the Free State and Northern Cape
provinces in South Africa (see also Okubamichael et al.
Figure 2. Number of mistletoe species that parasitize the most
common Acacia host species in southern Africa. Acacia karroo is
the most abundant host tree in South Africa and many types of
mistletoe species utilize this abundant species. However, in
Namibia, A. erioloba and A. mellifera are quite common and were
the most common hosts for mistletoes. In Zimbabwe, A. nigrescens
is common and is also highly utilized by mistletoe species in the
area (see van Wyk and van Wyk 1997 for the distribution pattern
of each Acacia species).
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2011a). The same species was found on the more abundant host species Boscia albitrunca and B. foetida in
Namibia. These results support the hypothesis that
mistletoe species that are host generalists across the entire range can be specific to particularly abundant hosts
on a local scale (e.g. Agelanthus natalitius, Phoradendron
leucarpum, Arceuthobium globosum and Viscum album).
Norton and de Lange (1999) found that this pattern is
also common in New Zealand mistletoes (Alepis flavida,
Peraxilla tetrapetala and P. colensoi) that parasitize only
the abundant species of Nothofagus.
Herbarium records showed that many mistletoe species tend to have one primary host species and use other
host species less frequently, at least in the South African
collections investigated. Even in the most generalist
mistletoes, not all available host genera are equally susceptible to infection by mistletoes at a given locality.
Usually mistletoes have a primary host genus that they
prefer or on which they become host-specific. This may
be linked to the existence of coevolutionary hotspots
where the interactions between mistletoes and their
hosts are strong. The mistletoes Plicosepalus kalachariensis and P. undulatus, for instance, parasitize only Acacia
species and may provide good examples of mistletoe
coevolution. Viscum menyharthii also parasitizes predominantly Acacia and Ficus species, even though Acacia
species are generally not the primary hosts for
Viscaceae.
We also found that mistletoe species are less likely to
share a single primary host genus, especially if they are
from different families. A Sørensen index (Sim) was used
to calculate the similarity in host genera use by the two
major mistletoe families. This index is calculated as 2C/
A þ B, where A ¼ number of species in sample A,
B ¼ number of species in sample B and C ¼ number of
species common in both A and B (see e.g. Magurran
1988). The Sørensen index comparing the host species
used by mistletoes in the Viscaceae and Loranthaceae
was low (Sim ¼ 0.26) with only 20 host genera shared between Loranthaceae and Viscaceae. This indicates that
mistletoe species in Viscaceae parasitize mainly host
genera that are not used by mistletoe species in
Loranthaceae and vice versa. For example, Euphorbia
and Olea are some of the most common host trees for
mistletoes in Viscaceae but they are not common hosts
for mistletoes in Loranthaceae. Additionally, even the
most generalist mistletoe species in Loranthaceae
(Tapinanthus oleifolius) and the most generalist mistletoe in Viscaceae (Viscum rotundifolium) had a low similarity index for host use (Sim ¼ 0.29). Viscum
rotundifolium does not utilize all 32 species of Acacia
that are reported to be parasitized by other mistletoes in
southern Africa, but instead only occurs on A. erioloba
AoB PLANTS www.aobplants.oxfordjournals.org
and A. karroo. These findings show clear trends for southern Africa that could be further tested by examining host
ranges in these two mistletoe families in North America
and Australia.
We have also observed that several mistletoe species
in the Walter Sisulu Botanical Garden (near
Johannesburg, South Africa, ca. 300 hectares) have a
non-overlapping domain of host species. In this particular site, if a host species is parasitized by a particular
mistletoe, it is unlikely to be parasitized by other mistletoe species occurring in the same habitat (Fig. 3). A negative co-occurrence pattern in mistletoe species that
specialize on distinct suites of host species has been also
reported in North America, New Zealand and Australia
(Hawksworth and Wiens 1972; Blick and Burns 2009;
Blick et al. 2012). Similarly, Fadini (2011) showed that
three congeneric and sympatric mistletoe species
(Psittacanthus biternatus, P. eucalyptifolius and P. plagiophyllus) specialize on different host species in the
Figure 3. We recorded four mistletoe species that reflect the general pattern of host specificity of mistletoes at Walter Sisulu
National Botanical Garden, Johannesburg, South Africa. The
mistletoes differ from being generalist to host-specific at the site.
Viscum rotundifolium was the generalist mistletoe species that
parasitizes at least six tree species, but it does not appear to parasitize tree species that are sole hosts for other co-occurring mistletoes. Agelanthus natalitius, has a limited number of host species
and predominantly parasitizes Acacia caffra. It is more rarely found
on Dombeya rotundifolia and Acacia karroo. Viscum combretum
mainly parasitizes Combretum erythrophyllum and rarely is found
on Dombeya rotundifolia. At the extreme end of host specificity,
Tapinanthus rubromarginatus parasitizes only Protea caffra.
Dashed circles of host trees indicate that they are rare at the location. Dashed lines that link the mistletoe–host interactions indicate
that the associated mistletoe seldom parasitizes those host trees.
The broader and darker lines indicate mistletoes that are specific
to the indicated host trees. The triangle shows that the mistletoes
range from host generalist (indicated by the base of the triangle)
to host-specific (indicated by the pointed end of the triangle)
species.
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Okubamichael et al. — Host specificity in mistletoes
Amazon. Mistletoes that are host-specific may have a
competitive edge over non-specific mistletoes where
several mistletoes coexist. For example, Jerome and
Ford (2002) suggested that host specificity in
Arceuthobium americanum reduces potential competition with other mistletoe species that may utilize the
same host species at a given site. A pattern of nonoverlap in mistletoe primary host use may be indicative
of competitive exclusion and could contribute to a geographic mosaic of mistletoe–host interactions. Such a
geographic mosaic could ultimately determine patterns
of host specificity in mistletoes (sensu Blick and Burns
2009). Further investigation is warranted to quantify the
degree of competition among mistletoe species and to
determine the mechanisms that drive such interactions.
At present, it is clear that there is a need to understand the complex networks of mistletoe–host interactions (Vidal-Russell and Nickrent 2008). Ecological
networks most frequently fit nested or modular patterns
(Genini et al. 2012). Networks that are nested contain a
few generalists that interact with one another and with
specialist species, which allows for the persistence of
specialists. In modular networks, generalist species form
sub-groups (modules) that interact more with the species within their module than they do with species in
other modules. Network analysis (a test of modularity
and nestedness) could be used to examine the structure
of patterns of mistletoe–host interactions at the population, species, genera and family levels (sensu Genini et al.
2012) [see Supporting Information—Appendix 1]. This
should be supplemented by a more comprehensive reciprocal transplant analysis and a genetic study.
Together, these investigations could reveal the underlying processes that are responsible for the development
and maintenance of mistletoe host specificity.
use a similar line of investigation to examine coevolution
in mistletoes and their host trees. On an evolutionary
time scale, mistletoes switch among different host species and the haustorium or other traits (e.g. stomata)
probably requires adaptive plasticity so that they can access nutrients and water from the prospective host speles et al. 2007).
cies (see Gonza
It would be ideal to test the geographic mosaic model
using reciprocal transplant experiments on a range of
host species and sites to determine differences in mistletoe fitness on different hosts (such as haustorium establishment, survival and reproduction). Reaction norms,
which are the pattern of phenotypes produced by a given
genotype under different environmental conditions,
could then be used to determine the selection pressure
in populations of mistletoes in different environments
(Yan 1993b; Lynch and Walsh 1998; Rödl and Ward
2002). Reciprocal transplant experiments on mistletoes
tend to result in low establishment success (Rödl and
Ward 2002), which require using large sample sizes.
Molecular markers could also be used to investigate genetic differentiation among populations. For example,
host race speciation in Tristerix (T. corymbosus to cactispecific T. aphyllus) was supported using molecular
phylogenetic methods (Amico et al. 2007; Amico and
Nickrent 2009).
A phylogenetic comparison of mistletoes and their
hosts could reveal the relative importance of coevolution
and host-switching events in mistletoe speciation (see
Jerome and Ford 2002). It would be important to determine whether mistletoes parasitize phylogenetically or
biogeographically similar hosts. The combined results of
these investigations would comprehensively test the
geographic mosaic model in order to explain the
mistletoe–host interaction at local and at larger geographic scales.
Future Directions
It would be useful to test whether the geographic specialization of mistletoes on different hosts results from
genetic divergence in preference hierarchies (phylogenetic host specificity) or ecological differences in the availability of hosts (specificity in geographic space). For
example, it is well known in animal parasites that some
populations exclusively parasitize one host for many
generations but do not lose their ability to recognize
other major hosts that they do not normally encounter
(Poulin 2010; Poulin et al. 2011; Cooper et al. 2012). On
the other hand, some animal parasites switch to new
hosts and lose their ability to infect the host species that
previously acted as a host. Currently, there are no data
on this subject in mistletoes and it would be important to
008
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Source of Funding
The National Research Foundation of South Africa and
the Claude Leon Foundation provided funding for this
research.
Contributions by the Authors
D.Y.O. reviewed the available information, and collected
and analyzed the required data for the paper. D.W. and
M.E.G. provided the supervision and contributed in conceptualization of the synthesis.
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Okubamichael et al. — Host specificity in mistletoes
Conflicts of Interest Statement
None declared.
Acknowledgements
We would like to thank Zivanai Tsvuura, Tiffany Pillay
and Timm Hoffman for their comments on earlier drafts.
We would also like to thank the National Research
Foundation of South Africa for funding D.W. and the
Claude Leon Foundation for funding M.E.G.
Supporting Information
The following additional information is available in the
online version of this article—
Appendix 1. Mistletoe species versus host species
interaction links. The species are ordered from generalist
to specialist (top to down). This network reflects some of
the herbarium specimens collected from Southern Africa
and stored mainly in the Bews Herbarium, Life Sciences,
PMB, UKZN.
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