Consuming and consumed: Biotic interactions of African mistletoes across different trophic levels

Katamssadan H . Tofel

1. Mistletoes use far more water per unit carbon fixed during photosynthesis than their hosts (i.e. they have lower 'water use efficiency', WUE). The widely cited 'nitrogen-parasitism hypothesis' posits that N is the most limiting resource for mistletoes and that they use their faster transpiration rates to acquire sufficient N from the host xylem. In a rather different context , the 'mimicry hypothesis' arose in the literature suggesting that some mistletoes mimic the morphology of host leaves in order to deploy higher N leaves without suffering higher levels of herbivory. These two non-exclusive hypotheses share the common goal of trying to explain patterns of mistletoe leaf N concentration. 2. We set out to test the generality of both hypotheses at broad geographic scale using data for 168 mistletoes–host pairs, from 39 sites, encompassing all continents except Antarctica. We drew together data from published literature and our own field data on two key plant functional traits, leaf N concentration (N mass) and leaf carbon isotopic composition (d 13 C) (representing long-term WUE and degree of stomatal control over photosynthesis). 3. Key findings included (i) little or no support for the N-parasitism hypothesis: differences in mistletoe and host N mass explained only 3% variation in differences in leaf d 13 C, and mistle-toe–host differences in leaf d 13 C were unrelated to whether or not the hosts were N-fixers (presumed to have higher N concentration in xylem sap); (ii) partial support for the mimicry hypothesis: mimic mistletoes generally had higher N mass when associated with N-fixing hosts (but, on non-N-fixing hosts there was no such pattern); and (iii) more broadly, mistletoes showed similar trait responses as their hosts to environmental drivers; for example, they showed similar-magnitude shifts in N mass and d 13 C in relation to site aridity. 4. Contrary to current belief, our findings suggest that nitrogen is not the limiting nutrient for mistletoes, at least not the main component driving the faster transpiration rates. Our results also give insight into the evolution of mimicry in mistletoes and show, for the first time, that mistletoes are also constrained by local water availability, exhibiting clear trait adaptations to environmental gradients. By reconsidering these issues at broad geographic scale and across a large number of species, our findings substantially modify current knowledge on the ecology and physiology of mistletoes and their hosts.

In a range of systems, studies on mistletoe distribution on the host plant have documented a number of factors that affect their occurrence and spread (Aukema & Martinez del Rio 2002a, Bowie & Ward 2004, Overton 1996, Reid et al. 1995). These patterns can be determined by host specificity, environmental conditions, host plant characteristics (Martinez del Rio et al. 1995) and the movement patterns of dispersal agents (Aukema & Martinez del Rio 2002a, 2002b). In mistletoe plants, host choice can be considerably influenced by the advantages of interacting with relatively abundant hosts (Norton & Carpenter 1998, Norton & De Lange 1999). Besides the relative abundance of host species, characteristics such as branch size, age and height can have a strong effect on mistletoe attachment resulting in size-related mistletoe infection patterns (Overton 1994). Generally positive relationships between mistletoe infection and host size have been demonstrated worldwide (Donohue 1995, Martinez del...

Received: 24 November 2021 | Revised: 5 April 2022 | 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 | 1103 1104 1 | | KRASYLENKO Et AL. 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 | 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 | 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. | 1107 1108 | KRASYLENKO Et AL. 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, | 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 | 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 | 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 | 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). | 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 REFERENCES Abba, C. C., Nduka, I., Eze, P. M., Ujam, T. N., Abonyi, D. O., & Okoye, F. B. C. (2016). Antimicrobial activity of secondary metabolites of endophytic Aspergillus species isolated from Loranthus micranthus. African Journal of Pharmaceutical Research & Development, 8(2), 136–140. Abreu, L. M.de, Almeida, A. R., Salgado, M., & Pfenning, L. H. (2010). Fungal endophytes associated with the mistletoe Phoradendron perrottettii and its host tree Tapirira guianensis. Mycological Progress, 9(4), 559–566. https://doi.org/10.1007/s11557- 010- 0663-8 Albert, S., Rhumeur, A., Rivière, J. L., Chauvrat, A., Sauroy-Toucouère, S., Martos, F., & Strasberg, D. (2017). Rediscovery of the mistletoe Bakerella hoyifolia subsp. bojeri (Loranthaceae) on Reunion Island: population status assessment for its conservation. Botany Letters, 164(3), 229–236. https://doi.org/10.1080/23818 107.2017.1340191 Álvarez-Pérez, S., & Herrera, C. M. (2013). Composition, richness and nonrandom assembly of culturable bacterial-microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiology Ecology, 83(3), 685–699. https://doi.org/10.1111/1574-6941.12027 Amutenya, A. T. (2017). Assessment of mistletoe – host interactions in a highland savanna in Windhoek, Namibia. A thesis submitted in fulfilment of the requirements for the degree of Master of Science of the University of Namibia (pp. 1–98). Atsalis, S. A. (2008). Natural history of the Brown Mouse Lemur (pp. 65–72). Routledge Balle, S. (1964a). Les Loranthacées de Madagascar et des archipels voisins. Adansonia, 4(1), 105–141. Balle, M. S. (1964b). Famille 60 – Loranthacées. In H. Humbert (Ed.), Flore de Madagascar et des Comores (plantes vasculaires) (pp. 1–124). Imprimerie officielle, Muséum national d'histoire naturelle. Baranyay, J. A. (1966). Fungi from dwarf mistletoe infections in western hemlock. Canadian Journal of Botany, 44(5), 597–604. https://doi. org/10.1139/b66- 071 Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology, 58, 1–21. https://doi.org/10.1002/ajp.10049 1115 Begoude, B. A. D., Slippers, B., Wingfield, M. J., & Roux, J. (2010). Botryosphaeriaceae associated with Terminalia catappa in Cameroon, South Africa and Madagascar. Mycological Progress, 9, 101–123. https://doi.org/10.1007/s11557- 009- 0622- 4 Bennett, R. E., Sillett, T. S., Rice, R. A., & Marra, P. P. (2021). Impact of cocoa agricultural intensification on bird diversity and community composition. Conservation Biology, 36, e13779. https://doi. org/10.1111/cobi.13779 Berg, G., Rybakova, D., Fischer, D., Cernava, T., Champomier Vergès, M. C., Charles, T., Chen, X., Cocolin, L., Eversole, K., Corral, G. H., Kazou, M., Kinkel, L., Lange, L., Lima, N., Loy, A., Macklin, J. A., Maguin, E., Mauchline, T., McClure, R., … Schloter, M. (2020). Microbiome definition re-visited: old concepts and new challenges. Microbiome, 8, 103. https://doi.org/10.1186/s4016 8020- 00875 - 0 Bitar, M. R., Pinto, V. D., Moreira, L. M., & Ribeiro, S. P. (2021). Gramnegative bacteria associated with a dominant arboreal ant species outcompete phyllosphere-associated bacteria species in a tropical canopy. Oecologia, 195, 959–970. https://doi.org/10.1007/s0044 2- 021- 04878-y Bollen, A., Elsacker, L., & Ganzhorn, J. (2004). Relations between fruits and disperser assemblages in a Malagasy littoral forest: A community-level approach. Journal of Tropical Ecology, 20(6), 599– 612. https://doi.org/10.1017/S0266 46740 4001853 Bollen, A., & Van Elsacker, L. (2002). Feeding ecology of Pteropus rufus (Pteropodidae) in the littoral forest of Sainte Luce, SE Madagascar. Acta Chiropterologica, 4(1), 33–47. https://doi. org/10.3161/001.004.0105 Bosque, C., Bosque, C. D., & Lloyd, P. (2017). Diet and time-activity budget of White-backed Mousebirds Colius colius in south-western South Africa, Ostrich. Journal of African Ornithology, 88(3), 1–6. https://doi.org/10.2989/00306525.2017.1294629 Boussim, I. J., Sallé, G., & Guinko, S. (1993). Tapinanthus parasite du karité au Burkina Faso. Bois Et Forets Des Tropiques, 238, 45–65. Braby, M. F. (2005). Afrotropical mistletoe butterflies: larval food plant relationships of Mylothris Hübner (Lepidoptera: Pieridae). Journal of Natural History, 39(6), 499–513. Brosset, A., & Erard, C. (1986). Les Oiseaux des Régions Forestières du Nord-est du Gabon. Volume 1. Écologie et comportment des espèces (pp. 1–289). Société Nationale de Protection de la Nature. Burns, A. E., Cunningham, S. A., & Watson, D. M. (2011). Arthropod assemblages in tree canopies: a comparison of orders on box mistletoe (Amyema miquelii) and its host eucalypts. Australian Journal of Entomology, 50(3), 221–230. https://doi. org/10.1111/j.1440-6055.2011.00811.x Byng, J. W., Smets, E. F., van Vugt, R., Bidault, E., Davidson, C., Kenicer, G., Chase, M. W., & Christenhusz, M. J. M. (2018). The phylogeny of angiosperms poster: A visual summary of APG IV family relationships and floral diversity. The Global Flora (pp. 4–7). Calvin, C. L., & Wilson, C. A. (1998). Comparative morphology of haustoria within African Loranthaceae. In R. Polhill & D. Wiens (Eds.), Mistletoes of Africa (pp. 17–36). The Royal Botanic Gardens. Calvin, C. L., & Wilson, C. A. (2006). Comparative morphology of epicortical roots in Old and New World Loranthaceae with reference to root types, origin, patterns of longitudinal extension and potential for clonal growth. Flora, 201(1), 51–64. https://doi.org/10.1016/j. flora.2005.03.001 Calvin, C. L., & Wilson, C. A. (2009). Epiparasitism in Phoradendron durangense and P. falcatum (Viscaceae). Aliso, 27(1), 1–12. https://doi. org/10.5642/aliso.20092701.02 Congdon, T. C. E., Bampton, I., & Collins, S. C. (2017). An illustrated report on the larvae, adults and host associations of 424 African Lepidoptera taxa belonging to the Papilionoidea. A second report of the Caterpillar Rearing Group of LepSoc Africa (pp. 1–124). 1116 | Cooney, S. J. N., Watson, D. M., & Young, J. (2006). Mistletoe nesting in Australian birds: A review. Emu Austral Ornithology, 106(1), 1–12. https://doi.org/10.1071/MU04018 Costa, J. M., Ramos, J. A., da Silva, L. P., Timoteo, S., Araújo, P. M., Felgueiras, M. S., Matos, A. R. C., Encarnação, P., Tenreiro, P. Q., & Heleno, P. H. (2014). Endozoochory largely outweighs epizoochory in migrating passerines. Journal of Avian Biology, 45, 59–64. https:// doi.org/10.1111/j.1600- 048X.2013.00271.x Craig, A. J. F. K. (2014). Nectar feeding by weavers (Ploceidae) and their role as pollinators. Ostrich, 85(1), 25–30. https://doi. org/10.2989/00306525.2014.900828 Crowley, B. E., Blanco, M. B., Arrigo-Nelson, S. J., & Irwin, M. T. (2013). Stable isotopes document resource partitioning and effects of forest disturbance on sympatric cheirogaleid lemurs. Naturwissenschaften, 100(10), 943–956. https://doi.org/10.1007/ s00114- 013-1094- 6 Davidar, P. (1983). Birds and neotropical mistletoe: effects on seedling recruitment. Oecologia, 60(2), 271–273. https://doi.org/10.1007/ BF00379532 Dibong, S. D., Din, N., Priso, R. J., Taffouo, V. D., Fankem, H., Salle, G., & Amougou, A. (2008). Parasitism of host trees by the Loranthaceae in the region of Douala (Cameroon). African Journal of Environmental Science & Technology, 2(11), 371–378. Dowsett-Lemaire, F. (1988). Fruit choice and seed dissemination by birds and mammals in the evergreen forests of upland Malawi. Revue d'Ecologie (Terre et Vie), 43, 251–285. Dzerefos, C. M., Witkowski, E. T. F., & Shackleton, C. M. (1998). Seedling survival, post-harvest recovery and growth rates of the woodrose-producing mistletoe Erianthemum dregei (Loranthaceae) on Sclerocarya birrea. South African Journal of Botany, 64(5), 303–307. Dzerefos, C. M., Witkowski, E. T. F., & Shackleton, C. M. (2003). Host-preference and density of woodrose-forming mistletoes (Loranthaceae) on savanna vegetation, South Africa. Plant Ecology, 167(1), 163–177. https://doi.org/10.1023/A:1023991514968 Ebada, S. S., Eze, P., Okoye, F. B., Esimone, C. O., & Proksh, P. (2016). The fungal endophyte Nigrospora oryzae produces quercetin monoglycosides previously known only from plants. Chemistry Select, 1(11), 2767–2771. https://doi.org/10.1002/slct.20160 0478 Egbewande, O., Jimoh, A. A., Ibitoye, E. B., & Olorede, B. R. (2011). Utilization of African Mistletoe (Tapinanthus bangwensis) leaf meal by broiler chickens. Pakistan Journal of Nutrition, 10(1), 19–22. https://doi.org/10.3923/pjn.2011.19.22 Ehleringer, J. R., Cook, C. S., & Tieszen, L. L. (1986). Comparative water use and nitrogen relationships in a mistletoe and its host. Oecologia, 68, 279–284. https://doi.org/10.1007/BF00384800 EOL. (2021). Encyclopedia of Life. Facilitated by the Smithsonian National Museum of Natural History. https://eol.org Feehan, J. (1985). Explosive flower opening in ornithophily: a study of pollination mechanisms in some Central African Loranthaceae. Botanical Journal of the Linnean Society, 90(2), 129–144. Gairola, S., Bhatt, A., Govender, Y., Baijnath, H., Procheş, Ş., & Ramdhani, S. (2013). Incidence and intensity of tree infestation by the mistletoe Erianthemum dregei (Eckl. & Zeyh.) V. Tieghem in Durban, South Africa. Urban Forestry & Urban Greening, 12(3), 315–322. https:// doi.org/10.1016/j.ufug.2013.03.012 Gill, F. B. (1971). Ecology and evolution of the sympatric Mascarene White-Eyes, Zosterops borbonica and Zosterops olivacea. The Auk, 88(1), 35–60. Gill, F. B., & Wolf, L. L. (1975). Foraging strategies and energetics of East African sunbirds at mistletoe flowers. The American Naturalist, 109(969), 491–510. Godfree, R. C., Tinnin, R. O., & Forbes, R. B. (2003). Relationships between Arceuthobium americanum and the structure of Pinus contorta var. murrayana stands in central Oregon. Plant Ecology, 165(1), 69–84. KRASYLENKO Et AL. Godschalk, S. (1985). Feeding behaviour of avian dispersers of mistletoe fruit in the Loskop Dam Nature Reserve, South Africa. South African Journal of Zoology, 20, 136–146. Godschalk, S. K. B. (1983a). The reproductive phenology of three mistletoe species in the Loskop Dam Nature Reserve, South Africa. South African Journal of Botany, 2(1), 9–14. Godschalk, S. K. B. (1983b). The morphology of some South African mistletoe fruits. South African Journal of Botany, 2(1), 52–56. Godschalk, S. K. L. (1983c). Mistletoe dispersal by birds in South Africa. In M. Calder & P. Bernhardt (Eds.), The biology of mistletoes (pp. 117– 128). Academic Press. Goelen, T., Sobhy, I. S., Vanderaa, C., de Boer, J. G., Delvigne, F., Francis, F., Wäckers, F., Rediers, H., Verstrepen, K. J., Wenseleers, T., Jacquemyn, H., & Lievens, B. (2020). Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid. Functional Ecology, 34(2), 507–520. https://doi.org/10.1111/1365-2435.13503 Green, A. K., Ward, D., & Griffiths, M. E. (2009). Directed dispersal of mistletoe (Plicosepalus acaciae) by Yellow-vented Bulbuls (Pycnonotus xanthopygos). Journal of Ornithology, 150(1), 167–173. https://doi. org/10.1007/s10336- 008- 0331-9 Griebel, A., Watson, D., & Pendall, E. (2017). Mistletoe, friend and foe: synthesizing ecosystem implications of mistletoe infection. Environmental Research Letters, 12(11), 115012. https://doi. org/10.1088/1748-9326/aa8fff Grímsson, F., Xafis, A., Neumann, F. H., Scott, L., Bamford, M. K., & Zetter, R. (2018). The first Loranthaceae fossils from Africa. Grana, 57(4), 249–259. https://doi.org/10.1080/00173134.2018.1430167 Guimarães, A. C., Siani, A. C., Bezerra, J. L., Souza, A. Q. L., & de Sarquis, M. I. M. (2013). Endophytic mycobiota characterization of the amazonian mistletoe Cladocolea micrantha hosted in cashew tree. American Journal of Plant Sciences, 4, 917–921. https://doi. org/10.4236/ajps.2013.44113 Hampel, L. D., Cheeptham, N., Flood, N. J., & Friedman, C. R. (2016). Plants, fungi, and freeloaders: examining temporal changes in the “taxonomic richness” of endophytic fungi in the dwarf mistletoe Arceuthobium americanum over its growing season. Botany, 95(3), 323–335. https://doi.org/10.1139/cjb-2016- 0240 Hansford, C. G. (1937). Annotated host list of Uganda parasitic fungi and plant diseases – Part III. The East African Agricultural Journal, 3(1), 79–84. https://doi.org/10.1080/03670 074.1937.11663731 Hansford, C. G. (1943). Host list of the parasitic fungi of Uganda: part II. The East African Agricultural Journal, 9(1), 50–55. https://doi. org/10.1080/03670 074.1943.11664317 Hódar, J. A., Lázaro-González, A., & Zamora, R. (2018). Beneath the mistletoe: parasitized trees host a more diverse herbaceous vegetation and are more visited by rabbits. Annals of Forest Science, 75, 77. https://doi.org/10.1007/s13595- 018- 0761-3 Hughes, S. J. (2007). Heteroconium and Pirozynskiella n. gen., with comments on conidium transseptation. Mycologia, 99(4), 628–638. https://doi.org/10.1080/15572536.2007.11832557 Irwin, M. T. (2008). Feeding ecology of Propithecus diadema in forest fragments and continuous forest. International Journal of Primatology, 29, 95–115. https://doi.org/10.1007/s1076 4- 007-9222-9 Irwin, M. T., Raharison, J. L., Raubenheimer, D. R., Chapman, C. A., & Rothman, J. M. (2015). The nutritional geometry of resource scarcity: effects of lean seasons and habitat disturbance on nutrient intakes and balancing in wild sifakas. PLoS One, 10(6), e0128046. https://doi.org/10.1371/journal.pone.0128046 Jami, F., Slippers, B., Wingfield, M. J., Loots, M. T., & Gryzenhout, M. (2015). Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecology, 15, 51–62. https://doi.org/10.1016/j.funeco.2015.03.001 Jordaan, A., Taylor, J. E., & Rossenkhan, R. (2006). Occurrence and possible role of endophytic fungi associated with seed pods of Colophospermum mopane (Fabaceae) in Botswana. South African KRASYLENKO Et AL. Journal of Botany, 72, 245–255. https://doi.org/10.1016/j. sajb.2005.09.007 Kalaiselvi, S., & Panneerselvam, A. (2021). Growth promotion utility of the plant microbiome. In D. Dhanasekaran, D. Paul, N. Amaresan, A. Sankaranarayanan, & Y. S. Shouche (Eds.), Microbiome-host interactions (pp. 307–319). CRC Press. Kaplin, B. A., Munyaligoga, V., & Moermond, T. C. (1998). The Influence of temporal changes in fruit availability on diet composition and seed handling in blue onkeys (Cercopithecus mitis doggetti). Biotropica, 30, 56–71. https://doi.org/10.1111/j.1744-7429.1998. tb00369.x Karadžić, D., & Lazarov, V. (2005). The most significant parasite and saprophyte fungi on mistletoe (Viscum album L.) and possibilities of their usage in bio-control. Bulletin of the Faculty of Forestry (University of Banja Luka), 3, 35–46 [in Serbian]. Kirkup, D. W. (1984). Avian visitors to some West African mistletoes. Golden Bough, 5, 3–4. Klopper, R. R., Gautier, L., Smith, G. F., Spichiger, R., & Chatelain, C. (2006). Inventory of the African flora: a world first for the forgotten continent: news & views. South African Journal of Science, 102(5), 185–186. Koffi, A. A., Kouassi, A. F., Kouadio, K., & Soro, D. (2020). Utilisation de quelques especes de Loranthaceae en pharmacopee traditionnelle par les populations locales de la region du Hambol dans le Nord de la Cote d'Ivoire. American Journal of Innovative Research & Applied Sciences, 10(1), 24–28. Kotan, R., Okutucu, A., Görmez, A. A., Karagoz, K., Dadasoglu, F., Karaman, İ., Hasanekoglu, İ., & Kordali, Ş. (2013). Parasitic bacteria and fungi on common mistletoe (Viscum album L.) and their potential application in biocontrol. Journal of Phytopathology, 161, 165– 171. https://doi.org/10.1111/jph.12048 Krasylenko, Y., Těšitel, J., Ceccantini, G., Oliveira-da-Silva, M., Dvořák, V., Steele, D., Sosnovsky, Y., Piwowarczyk, R., Watson, D. M., & Teixeira-Costa, L. (2021). Parasites on parasites: Hyper-, epi-, and autoparasitism among flowering plants. American Journal of Botany, 108(1), 8–21. https://doi.org/10.1002/ajb2.1590 Kuijt, J. (1969). The biology of parasitic flowering plants. University of California Press. Kuijt, J., & Hansen, B. (2015). Flowering plants, Eudicots: Santalales, Balanophorales. In K. Kubitzki (Ed.), The families and genera of vascular plants, vol. 12 (pp. 1–213). Springer. Kyalangalilwa, B., Boatwright, J. S., Daru, B. H., Maurin, O., & van der Bank, M. (2013). Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Botanical Journal of the Linnean Society, 172, 500–523. https://doi.org/10.1111/boj.12047 Ladoh-Yemeda, C. F., Nyegue, M. A., Ngene, J. P., Benelesse, G. E., Lenta, B., Wansi, J. D., Mpondo, E., & Dibong, S. D. (2015). Identification and phytochemical screening of endophytic fungi from stems of Phragmanthera capitata (Sprengel) S. Balle (Loranthaceae). Journal of Applied Biosciences, 90, 8355–8360. Lahann, P. (2007). Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. Journal of Zoology, 271, 88–98. Lázaro-González, A., Gargallo-Garriga, A., Hódar, J. A., Sardans, J., Oravec, M., Urban, O., Peñuelas, J., & Zamora, R. (2021). Implications of mistletoe parasitism for the host metabolome: A new plant identity in the forest canopy. Plant, Cell & Environment, 44, 3655–3666. https://doi.org/10.1111/pce.14179 Lázaro-González, A., Hódar, J. A., & Zamora, R. (2017). Do the arthropod communities on a parasitic plant and its hosts differ? European Journal of Entomology, 114, 215–221. Lázaro-González, A., Hódar, J. A., & Zamora, R. (2020). Ecological assembly rules on arthropod community inhabiting mistletoes. Ecological Entomology, 45(5), 1088–1098. | 1117 Linnakoski, R., Puhakka-Tarvainen, H., & Pappinen, A. (2012). Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecology, 5, 298–308. https://doi.org/10.1016/j.funeco.2011.08.006 Liu, B., Chi, T. L., Barrett, R. L., Nickrent, D. L., Zhiduan, C., Limin, L., & Vidal-Russell, R. (2018). Historical Biogeography of Loranthaceae (Santalales): Diversification Agrees with Emergence of Tropical Forests and Radiation of Songbirds. Molecular Phylogenetics & Evolution, 124, 199–212. https://doi.org/10.1016/j. ympev.2018.03.010 Lompo, O., Dimobe, K., Mbayngone, E., Savadogo, S., Sambaré, O., Thiombiano, A., & Ouédraogo, A. (2021). Climate influence on the distribution of the yellow plum (Ximenia Americana L.) in Burkina Faso. Trees, Forests & People, 4, 100072. https://doi.org/10.1016/j. tfp.2021.100072 Marshall, J. D., Ehleringer, J. R., Schulze, E. D., & Farquhar, G. (1994). Carbon isotope composition, gas exchange, and heterotrophy in Australian mistletoes. Functional Ecology, 8, 237–241. Martin, L. L., Cynthia, M., Friedman, R., & Phillips, L. A. (2012). Fungal Endophytes of the obligate parasitic dwarf mistletoe Arceuthobium americanum (Santalaceae) act antagonistically in vitro against the native fungal pathogen Cladosporium (Davidiellaceae) of their host. American Journal of Botany, 99(12), 2027–2034. https://doi. org/10.3732/ajb.1200189 Martínez del Rio, C., Silva, A., Medel, R., & Hourdequin, M. (1996). Seed dispersers as disease vectors: Bird transmission of mistletoe seeds to plant hosts. Ecology, 77, 912–921. Mathiasen, R. L., Nickrent, D. L., Shaw, D. C., & Watson, D. M. (2008). Mistletoes: pathology, systematics, ecology, and management. Plant Disease, 92, 988–1006. Maul, K., Krug, M., Nickrent, D. L., Müller, K. F., Quandt, D., & Wicke, S. (2019). Morphology, geographic distribution, and host preferences are poor predictors of phylogenetic relatedness in the mistletoe genus Viscum L. Molecular Phylogenetics & Evolution, 131, 106–115. https://doi.org/10.1016/j.ympev.2018.10.041 McGee, E., & Vaughn, S. (2017). Of lemurs and louse flies: The biogeochemical and biotic effects of forest disturbance on Propithecus edwardsi and its obligate ectoparasite Allobosca crassipes in Ranomafana National Park, southeastern Madagascar. American Journal of Primatology, 79(8), 1–12. https://doi.org/10.1002/ ajp.22676 Mellado, A., Morillas, L., Gallardo, A., & Zamora, R. (2016). Temporal dynamic of parasite mediated linkages between the forest canopy and soil processes and the microbial community. New Phytologist, 211(4), 1382–1392. https://doi.org/10.1111/nph.13984 Mellado, A., & Zamora, R. (2014). Generalist birds govern the seed dispersal of a parasitic plant with strong recruitment constraints. Oecologia, 176, 139–147. https://doi.org/10.1007/s0044 2- 014-3013-8 Mellado, A., & Zamora, R. (2016). Spatial heterogeneity of a parasitic plant drives the seed dispersal pattern of a zoochorous plant community in a generalist dispersal system. Functional Ecology, 30, 459– 467. https://doi.org/10.1111/1365-2435.12524 Mellado, A., & Zamora, R. (2017). Parasites structuring ecological communities: the mistletoe footprint in mediterranean pine forests. Functional Ecology, 31, 2167–2176. https://doi. org/10.1111/1365-2435.12907 Midgley, J. J., & Joubert, D. (1991). Mistletoes, their host plants and the effects of browsing by large mammals in Addo Elephant National Park. Koedoe, 34(2), 149–152. https://doi.org/10.4102/koedoe. v34i2.430 Mokotjomela, T. M., Musil, C. F., & Esler, K. J. (2013). Potential seed dispersal distances of native and non-native fleshy fruiting shrubs in the South African Mediterranean climate region. Plant Ecology, 214(9), 1127–1137. Molvray, M., Kores, P. J., & Chase, M. W. (1999). Phylogenetic relationships within Korthalsella (Viscaceae) based on nuclear ITS and 1118 | plastid trnL-F sequence data. American Journal of Botany, 86(2), 249– 260. https://doi.org/10.2307/2656940 Ndagurwa, H. G., Dube, J. S., Mlambo, D., & Mawanza, M. (2014). The influence of mistletoes on the litter-layer arthropod abundance and diversity in a semi-arid savanna, Southwest Zimbabwe. Plant & Soil, 383(1), 291–299. https://doi.org/10.1007/s1110 4- 014-2176-8 Ndagurwa, H. G., Maponga, T. S., & Muvengwi, J. (2020). Mistletoe litter accelerates the decomposition of recalcitrant host litter in a semiarid savanna, south-west Zimbabwe. Austral Ecology, 45(8), 1080– 1092. https://doi.org/10.1111/aec.12935 Ndagurwa, H. G., Nyawo, E., & Muvengwi, J. (2016). Use of mistletoes by the Grey Go-away-bird (Corythaixoides concolor, Musophagidae) in a semi-arid savannah, south-west Zimbabwe. African Journal of Ecology, 54(3), 336–341. https://doi.org/10.1111/aje.12334 Ndagurwa, H. G. T., & Dube, J. S. (2013). Nutritive value and digestibility of mistletoes and woody species browsed by goats in a semi-arid savanna, southwest Zimbabwe. Livestock Science, 151(2–3), 163– 170. https://doi.org/10.1016/j.livsci.2012.10.020 Nickrent, D. L. (2002). Plantas parásitas en el mundo [Parasitic plants of the world]. In J. A. López-Saez, P. Catalán, & L. Sáez (Eds.), Plantas parásitas de la Península Ibérica e Islas Baleares (pp. 7–27). Mundi-Prensa. Nickrent, D. L., Malécot, V., Vidal-Russell, R., & Der, J. P. (2010). A revised classification of Santalales. Taxon, 59(2), 538–558. https:// doi.org/10.1002/tax.592019 Norton, D. A., & Carpenter, M. A. (1998). Mistletoes as parasites: Host specificity and speciation. Trends in Ecology & Evolution, 13, 101– 105. https://doi.org/10.1016/S0169-5347(97)01243-3 Noutcheu, R., Tchatat, M., Mony, R., Mokake, E. S., Taffouo, V. D., & Dibong, S. D. (2013). Phenology, parasitism of Phragmantera capitata and myrmecofauna associated to host trees at the orchard of the chiet's palace Ndogbong (Douala, Cameroon). Agriculture & Biology Journal of North America, 4(5), 539–551. Okubamichael, D. Y., Griffiths, M. E., & Ward, D. (2011). Host specificity, nutrient and water dynamics of the mistletoe Viscum rotundifolium and its potential host species in the Kalahari of South Africa. Journal of Arid Environments, 75(10), 898–902. https://doi.org/10.1016/j. jaridenv.2011.04.026 Okubamichael, D. Y., Griffiths, M. E., & Ward, D. (2014). Reciprocal transplant experiment suggests host specificity of the mistletoe Agelanthus natalitius in South Africa. Journal of Tropical Ecology, 30, 153–163. https://doi.org/10.1017/S0266 467413000801 Okubamichael, D. Y., Griffiths, M. E., & Ward, D. (2016). Host specificity in parasitic plants—perspectives from mistletoes. AoB PLANTS, 8, plw069. Okubamichael, D. Y., Rasheed, M. Z., Griffiths, M. E., & Ward, D. (2011). Avian consumption and seed germination of the hemiparasitic mistletoe Agelanthus natalitius (Loranthaceae). Journal of Ornithology, 152, 643–649. https://doi.org/10.1007/s10336- 010- 0624-7 Ondoua, J. M., Mony, R., Dibong, S. D., Ngotta, B. J. B., Taffouo, V. D., Kenne, M., & Ekodeck, G. E. (2016). Myrmecofauna of cocoa trees infested by Loranthaceae genus Phragmanthera in Sodecao seed fields of Nkoemvone (South of Cameroon). Journal of Entomology & Nematology, 8(3), 19–27. Oosthuizen, D., & Balkwill, K. (2018). Viscum songimveloensis, a new species of mistletoe from South Africa. South African Journal of Botany, 115, 194–198. https://doi.org/10.1016/j.sajb.2018.02.004 Oriola, A. O., Aladesanmi, A. J., Akinkunmi, E. O., & Olawuni, I. J. (2020). Antioxidant and antimicrobial studies of some hemi-parasitic West African plants. European Journal of Medicinal Plants, 31, 17–26. https://doi.org/10.9734/EJMP/2020/v31i330219 Peršoh, D. (2013). Factors shaping community structure of endophytic fungi – Evidence from the Pinus-Viscum-system. Fungal Diversity, 60, 55–69. https://doi.org/10.1007/s13225- 013- 0225-x Peršoh, D., Melcher, M., Flessa, F., & Rambold, G. (2010). First fungal community analyses of endophytic ascomycetes associated with Viscum KRASYLENKO Et AL. album ssp. austriacum and its host Pinus sylvestris. Fungal Biology, 114(7), 585–596. https://doi.org/10.1016/j.funbio.2010.04.009 Philcox, D. (1982). Loranthacées [Loranthaceae]. In Flore des Mascareignes: La Réunion, Maurice, Rodrigues. 153 Lauracées à 160 Euphorbiacées [Flora of Mascarenes: La Reunion, Mauritius, Rodrigues. 153 Lauraceae to 160 Euphorbiaceae]. MSIRI, ORSTOM, IRD éditions, and RBG. Pirttilä, A. M., Joensuu, P., Pospiech, H., Jalonen, J., & Hohtola, A. (2004). Bud endophytes of Scots pine produce adenine derivatives and other compounds that affect morphology and mitigate browning of callus cultures. Physiologia Plantarum, 121(2), 305–312. https://doi. org/10.1111/j.0031-9317.2004.00330.x Poczai, P., Varga, I., & Hyvönen, J. (2015). Internal transcribed spacer (ITS) evolution in populations of the hyperparasitic European mistletoe pathogen fungus, Sphaeropsis visci (Botryosphaeriaceae): The utility of ITS2 secondary structures. Gene, 558(1), 54–64. https:// doi.org/10.1016/j.gene.2014.12.042 Polhill, R. (1989). Speciation patterns in African Loranthaceae. In L. B. HolmNielsen, I. C. Nielsen, & H. Balslev (Eds.), Tropical forests: Botanical dynamics, speciation and diversity (pp. 221–236). Academic Press. Polhill, R., & Wiens, D. (1998). Mistletoes of Africa. Royal Botanic Gardens. Polhill, R., & Wiens, D. (1999a). Loranthaceae. In H. J. Beentje & C. M. Whitehouse (Eds.), Flora of tropical East Africa (pp. 1–30). A.A. Balkema. Polhill, R., & Wiens, D. (1999b). Viscaceae. In H. J. Beentje & C. M. Whitehouse (Eds.), Flora of tropical East Africa (pp. 1–24). A.A. Balkema. Ponzio, C., Gols, R., Pieterse, C. M. J., & Dicke, M. (2013). Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Functional Ecology, 27(3), 587–598. https://doi.org/10.1111/1365-2435.12035 Powzyk, J. A., & Mowry, C. B. (2003). Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. International Journal of Primatology, 24, 1143–1162. https://doi. org/10.1023/B:IJOP.00000 05984.36518.94 Prado, A., Marolleau, B., Vaissière, B. E., Barret, M., & Torres-Cortes, G. (2020). Insect pollination: An ecological process involved in the assembly of the seed microbiota. Scientific Reports, 10, 3575. https:// doi.org/10.1038/s41598- 020-60591-5 Qian, C. D., Fu, Y. H., Jiang, F. S., Xu, Z. H., Cheng, D. Q., Ding, B., Gao, C. X., & Ding, Z. S. (2014). Lasiodiplodia sp. ME4-2, an endophytic fungus from the floral parts of Viscum coloratum, produces indole-3carboxylic acid and other aromatic metabolites. BMC Microbiology, 14, 297. https://doi.org/10.1186/s12866- 014- 0297- 0 Raherilalao, M. J., & Goodman, S. M. (2011). Histoire Naturelle des Familles et Sous-familles Endémiques d'Oiseaux de Madagascar. Series: Guides sur la Diversité Biologique de Madagascar (vol. 3, 148 p.). Raji, I. A., Chaskda, A. A., Manu, S. A., & Downs, C. (2021). Bird species use of Tapinanthus dodoneifolius mistletoes parasitising African locust bean trees Parkia biglobosa in Amurum Forest Reserve, Nigeria. Journal of Ornithology, 162, 1129–1140. https://doi.org/10.1007/ s10336- 021- 01890 - 0 Rakotomanana, H., & Rene de Roland, L. A. (2004). Breeding ecology of the endemic, Madagascan, Velvet Asity Philepitta castanea. Ornithological Science, 6, 79–85. Ran, J.-H., Shen, T. T., Wang, M. M., & Wang, X. Q. (2018). Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms. Proceedings of the Royal Society B: Biological Sciences, 285, 20181012. https://doi.org/10.1098/rspb.2018.1012 Reid, N. (1989). Dispersal of mistletoe by honeyeaters and flowerpeckers: Components of seed dispersal quality. Ecology, 70, 137–145. Reid, N. (1990). Mutualistic interdependence between mistletoe (Amyema quandang), and spiny-cheeked honeyeaters and mistletoe birds in an arid woodland. Australian Journal of Ecology, 15, 175–190. Reid, N. (1991). Coevolution of mistletoes and frugivorous birds. Australian Journal of Ecology, 16, 457–469. | KRASYLENKO Et AL. Rering, C. C., Vannette, R. L., Schaeffer, R. N., & Beck, J. J. (2020). Microbial co-occurrence in floral nectar affects metabolites and attractiveness to a generalist pollinator. Journal of Chemical Ecology, 46, 659–667. https://doi.org/10.1007/s10886- 020- 01169-3 Ribeiro, F. S. L., da Costa Garcia, A., Dias dos Santos, H. E., Montoya, Q. V., Rodrigues, A., de Oliveira, J. M., & de Oliveira, C. M. (2018). Antimicrobial activity of crude extracts of endophytic fungi from Oryctanthus alveolatus (Kunth) Kuijt (Mistletoe). African Journal of Microbiology Research, 12(11), 263–268. https://doi.org/10.5897/ AJMR2017.8772 Room, P. M. (1971). Some Physiological Aspects of the Relationship between Cocoa, Theobroma cacao, and the Mistletoe Tapinanthus bangwensis (Engl. and K. Krause). Annals of Botany, 35(1), 169–174. https://doi.org/10.1093/oxfordjournals.aob.a084457 Room, P. M. (1972a). The constitution and natural history of the fauna of the mistletoe Tapinanthus bangwensis (Engl. & K. Krause) growing on cocoa in Ghana. The Journal of Animal Ecology, 41, 519–535. Room, P. M. (1972b). The fauna of the mistletoe Tapinanthus bangwensis (Engl. & K. Krause) growing on cocoa in Ghana: relationships between fauna and mistletoe. The Journal of Animal Ecology, 41, 611–621. Room, P. M. (1973). Ecology of the Mistletoe Tapinanthus Bangwensis Growing on Cocoa in Ghana. Journal of Ecology, 61(3), 729–742. Roxburgh, L. (2007). The effect of gut processing on the quality of mistletoe seed dispersal. Journal of Tropical Ecology, 23(3), 377–380. https://doi.org/10.1017/S0266 467407004014 Roxburgh, L., & Nicolson, S. W. (2005). Patterns of host use in two African mistletoes: the importance of mistletoe–host compatibility and avian disperser behaviour. Functional Ecology, 19, 865–873. https://doi.org/10.1111/j.1365-2435.2005.01036.x Roxburgh, L., & Nicolson, S. W. (2008). Differential dispersal and survival of an African mistletoe: does host size matter? Plant Ecology, 195(1), 21–31. https://doi.org/10.1007/s11258- 007-9295-8 Schiestl, F. P. (2015). Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytologist, 206(2), 571–577. https://doi.org/10.1111/nph.13243 Shamoun, S. F., Ramsfield, T. D., & van der Kamp, B. J. (2003). Biological control approach for management of dwarf mistletoes. New Zealand Journal of Forest Science, 33(3), 373–384. Soyer-Poskin, D., & Schmizt, A. (1962). Phanerogames parasites et hemiparasites des arbres des environs d'Elisabethville (Katanga). Lejeunia, Nouvelle Serie, 7, 1–50. Stevens, P.F. (2001). Angiosperm phylogeny website. Version 14, July 2017 [and more or less continuously updated since]. http://www.mobot. org/MOBOT/research/APweb/ Sun, C., & Moermond, T. C. (1997). Foraging ecology of three sympatric turacos in a montane forest in Rwanda. Auk, 114(3), 396–404. https://doi.org/10.2307/4089241 Tanaka, A., Tapper, B. A., Popay, A., Parker, E. J., & Scott, B. (2005). A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Molecular Microbiology, 57(4), 1036–1050. https://doi.org/10.1111/j.1365-2958.2005.04747.x Teixeira-Costa, L., Ocampo, G., & Ceccantini, G. (2020). Morphogenesis and evolution of mistletoes' haustoria. In D. Demarco (Ed.), Plant ontogeny (pp. 107–157). Nova Science Publishers. Těšitel, J., Li, A. R., Knotková, K., McLellan, R., Bandaranayake, P. C., & Watson, D. M. (2021). The bright side of parasitic plants: what are they good for? Plant Physiology, 185(4), 1309–1324. The Angiosperm Phylogeny Group. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1–20. https://doi.org/10.1111/boj.12385 Tizhe, T.D., Alonge, S.O., & Aliyu, R.E. (2016). Mistletoe presence on five tree species of Samaru area, Nigeria. African Journal of Plant Science, 10(1), 16–22. 1119 Toghueo, R. M. K., Zabalgogeazcoa, I., Vázquez de Aldana, B. R., & Boyom, F. F. (2017). Enzymatic activity of endophytic fungi from the medicinal plants Terminalia catappa, Terminalia mantaly and Cananga odorata. South African Journal of Botany, 109, 146–153. https://doi. org/10.1016/j.sajb.2016.12.021 Tudzynski, B. (1997). Fungal phytohormones in pathogenic and mutualistic associations. Plant Relationships, 5, 167–184. Varga, I., Poczai, P., Cernák, I., & Hyvönen, J. (2014). Application of direct PCR in rapid rDNA ITS haplotype determination of the hyperparasitic fungus Sphaeropsis visci (Botryosphaeriaceae). Springerplus, 3, 569. https://doi.org/10.1186/2193-1801-3-569 Vidal-Russell, R., & Nickrent, D. L. (2008). Evolutionary relationships in the showy mistletoe family (Loranthaceae). American Journal of Botany, 95(8), 1015–1029. https://doi.org/10.3732/ajb.0800085 Walsberg, G. E. (1975). Digestive adaptation of Phainopepela nitens associated with the eating mistletoe berries. The Condor, 77, 169–174. Watson, D. M. (2001). Mistletoe – A keystone resource in forests and woodlands worldwide. Annual Review of Ecology and Systematics, 32, 219– 249. https://doi.org/10.1146/annurev.ecolsys.32.081501.114024 Watson, D. M., Cook, M., & Fadini, R. F. (2020). Towards best-practice management of mistletoes in horticulture. Botany, 98(9), 489–498. https://doi.org/10.1139/cjb-2019- 0205 Watson, D. M., & Herring, M. (2012). Mistletoe as a keystone resource: an experimental test. Proceedings of the Royal Society B: Biological Sciences, 279, 3853–3860. Watson, D. M., & Rawsthorne, J. (2013). Mistletoe specialist frugivores: Latterday ‘Johnny Appleseeds’ or self-serving market gardeners? Oecologia, 172(4), 925–932. https://doi.org/10.1007/s0044 2- 013-2693-9 Weston, K. A. (2009). Mistletoe reproductive mutualisms in a West African montane forest. M.Sc. thesis, University of Canterbury (pp. 1–141). Weston, K. A., Chapman, H. M., Kelly, D., & Moltchanova, E. V. (2012). Dependence on sunbird pollination for fruit set in three West African montane mistletoe species. Journal of Tropical Ecology, 28(2), 205–213. https://doi.org/10.1017/S0266 46741100068X Wicker, F., & Shaw, G. C. (1968). Fungal parasites of dwarf mistletoes. Mycologia, 60(2), 372–383. https://doi.org/10.1080/00275 514.1968.12018578 Wilson, C. A., & Calvin, C. L. (2017). Metadata provide insights on patterns of epiparasitism in mistletoes (Santalales), an overlooked topic in forest biology. Botany, 95(3), 259–269. https://doi.org/10.1139/ cjb-2016- 0264 Zamora, R., Lázaro-González, A., & Hódar, J. A. (2020). Secondary foundation species foster novel plant-animal interactions in the forest canopy: evidence from mistletoe. Insect Conservation & Diversity, 13(5), 470–479. https://doi.org/10.1111/icad.12428 Zuria, I., Castellanos, I., & Gates, J. E. (2014). The influence of mistletoes on birds in an agricultural landscape of central Mexico. Acta Oecologica, 61, 51–56. https://doi.org/10.1016/j.actao.2014.10.004 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

RELATED PAPERS

RELATED TOPICS

Log In

Consuming and consumed: Biotic interactions of African mistletoes across different trophic levels

Consuming and consumed: Biotic interactions of African mistletoes across different trophic levels

Related Papers

RELATED PAPERS

RELATED TOPICS