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Seed Dispersal Syndromes in the Madagascan Flora: the Unusual Importance of Primates

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Seed Dispersal Syndromes in the Madagascan Flora: the Unusual Importance of Primates Seed dispersal syndromes in the Madagascan flora: the unusual importance of primates A URÉLIE A LBERT-DAVIAUD,SARAH P ERILLO and W OLFGANG S TUPPY Abstract Madagascar is one of the most threatened bio- Dewar & Richard, ; Ali & Krause, ), sympatric spe- diversity hotspots, and protection of its biodiversity is be- ciation (Buerki et al., ) and relatively recent climate coming increasingly urgent as deforestation of the island changes (Yoder & Nowak, ; Buerki et al., ; continues. For the long-term success of conservation efforts Mercier & Wilmé, ). Levels of endemism are as high it is essential that key ecological processes, such as seed dis- as % in vascular plants (Callmander et al., ) and persal, are protected and restored. Therefore, the identifica- % in vertebrates (Goodman & Benstead, ). With on- tion of ecological gaps is a vital task. For Madagascar, only going deforestation, Madagascar’s unique biodiversity is little is known about plant–animal interactions, and trad- highly threatened (Brooks et al., ). itional methods of ecological research are too time-consum- Deforestation inevitably causes defaunation. Both pro- ing to provide crucial information about breakdowns in cesses result in imbalanced, disturbed or even dysfunctional these interactions. To identify likely dispersal gaps we there- ecosystems. A critical consequence, which has so far re- fore used a theoretical approach to analyse plant–disperser ceived little attention from conservationists, is the break- interactions in Madagascar. We used data science tools to down of key plant–animal interactions, such as seed impute missing data on relevant plant traits to subsequently dispersal. The extinction of animal dispersers has cata- predict the most likely dispersal agents for each of strophic consequences for the long-term survival of animal- Madagascar’s endemic plant species. We found that % dispersed plant species (Howe & Smallwood, ; Herrera, of the endemic species (N = ,) are endozoochorous, ; Caughlin et al., ). Plant regeneration is limited in and among these –% display a primate syndrome and the absence of seed dispersers, resulting in an increasing ag- –% a bird syndrome (depending on the definition of syn- gregation of individuals and a strongly increasing probabil- dromes). This lower percentage of endozoochorous species ity of extinction (Terborgh et al., ; Caughlin et al., ). and higher percentage of species with a primate syndrome Long-term conservation can therefore be successful only if in Madagascar compared to other tropical areas reflects the gaps in dispersal mutualisms are identified and repaired. unusual disperser guild on the island. Only five bird species For Madagascar, knowledge about plant species and but lemur species are frugivorous, and of those lemur plant–animal interactions is still scarce, and deforestation species are currently threatened with extinction. The dis- and defaunation are progressing rapidly. Traditional meth- appearance of frugivorous lemurs would significantly change ods of studying ecological processes such as seed dispersal the vegetation dynamics of Madagascar’s ecosystems, and a (e.g. long-term field observations) are too time-consuming high proportion of Madagascar’s endemic plants would to provide comprehensive information about the breakdown enter an extinction vortex. of vital plant–animal interactions. Dispersal syndromes (i.e. sets of fruit or seed traits) provide a practical concept for pre- Keywords Bird, dispersal spectra, endozoochory, Madagascar, dicting plant–animal interactions and interdependencies in a ornithochory, primate, primatochory, seed dispersal community quickly and accurately (van der Pijl, ;Howe, Supplementary material for this article is available at ; Kuhlmann & Ribeiro, ). In the absence of compre- https://doi.org/./S hensive data to infer dispersal syndromes in Madagascan ecosystems, we used data science tools to impute missing data on relevant plant traits. Using this approach we were able to assign dispersal syndromes to Madagascar’sendemic Introduction plant species and to infer vital plant–animal relationships adagascar is one of the most threatened biodiversity and interdependencies. Mhotspots (Brooks et al., ). Most of the island’s Of the various dispersal strategies plants have evolved, plant and animal species are endemic as a result of its endozoochory is usually the most common in tropical and long isolation from other continents (c. million years; subtropical rainforests, where at least % but more often –% of tree species bear fleshy fruits (Howe & Smallwood, ; Jordano, ; Willson & Traveset, AURÉLIE ALBERT-DAVIAUD (Corresponding author), SARAH PERILLO and WOLFGANG ; Osuri et al., ). Diaspores of endozoochorous spe- STUPPY Royal Botanic Gardens, Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, UK. E-mail [email protected] cies generally offer an edible reward to attract animal disper- Received July . Revision requested September . sers (e.g. fruit pulp, elaiosomes or arils). The predominance Accepted October . First published online February . of a syndrome is not always proportional to the abundance Oryx, 2018, 52(3), 418–426 © 2018 Fauna & Flora International doi:10.1017/S0030605317001600 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 01 Oct 2021 at 14:25:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605317001600 Seed dispersal in the Madagascan flora 419 of the corresponding dispersal agent in a community TABLE 1 Extant frugivores in Madagascar. Only species for which (Hughes et al., ; Herrera, ); however, Madagascar fruits constitute the largest component of their diet during most is unique in that its extant frugivorous guild is strikingly of the year are included; granivores are excluded. Data from small compared to other tropical areas (Goodman & Goodman & Benstead ( ), IUCN ( ) and Mittermeier et al. (). Ganzhorn, ; Ganzhorn et al., ). Only lemur, three bat, five bird and one tortoise species on the island Species Family Conservation status are mainly frugivorous (excluding granivores) (Table ). Bats Therefore, an analysis of the frequency of the various seed Eidolon dupreanum Pteropodidae Vulnerable dispersal strategies present in Madagascar’s endemic plant Pteropus rufus Pteropodidae Vulnerable species (i.e. seed dispersal spectra; Hughes et al., ) Rousettus Pteropodidae Near Threatened madagascariensis would be informative. The proportion of frugivorous species Birds in Madagascar has always been small, even before the Alectroenas Columbidae Least Concern Holocene extinctions (Godfrey et al., ). Hypotheses to madagascariensis explain the unusually low number of frugivores include the Hypsipetes Pycnonotidae Least Concern unpredictable pattern of fruit production on the island madagascariensis (Goodman & Ganzhorn, ; Wright, ) and the Philepitta castanea Philepittidae Least Concern lower absolute abundance of fruiting trees at any given Philepitta schlegeli Philepittidae Near Threatened Treron australis Columbidae Least Concern time compared to other tropical areas (Federman et al., Primates ). The most unusual aspect of Madagascar’s disperser Cheirogaleus major Cheirogaleidae Data Deficient guild is that there are only five species of frugivorous birds Cheirogaleus medius Cheirogaleidae Least Concern on the island, whereas in other tropical areas birds are the Eulemur albifrons Lemuridae Endangered most important and diverse group of frugivores (Fleming Eulemur cinereiceps Lemuridae Critically et al., ). Endangered Our aim was to answer the following questions: ()Is Eulemur collaris Lemuridae Endangered the small size of Madagascar’s disperser guild reflected in Eulemur coronatus Lemuridae Endangered a lower than average proportion of endozoochorous plant Eulemur flavifrons Lemuridae Critically Endangered species compared to other tropical areas? ( ) Is the low Eulemur fulvus Lemuridae Near Threatened ’ proportion of birds among Madagascar s seed dispersers Eulemur macaco Lemuridae Vulnerable reflected in a lower than average proportion of species Eulemur mongoz Lemuridae Critically with a bird dispersal syndrome compared to other tropical Endangered areas? () Is there a difference in the frequencies of Eulemur rubriventer Lemuridae Vulnerable dispersal syndromes between Madagascar’s various Eulemur rufifrons Lemuridae Near Threatened bioclimates and vegetation formations? Generally, forests Eulemur rufus Lemuridae Vulnerable Eulemur sanfordi Lemuridae Endangered and humid areas harbour a higher proportion of Lemur catta Lemuridae Endangered endozoochorous species than open vegetation (e.g. grass- Microcebus murinus Cheirogaleidae Least Concern lands) and dry areas (Howe & Smallwood, ; Willson Microcebus myoxinus Cheirogaleidae Vulnerable et al., ). Microcebus rufus Cheirogaleidae Vulnerable Varecia rubra Lemuridae Critically Endangered Varecia variegata Lemuridae Critically Methods Endangered Reptiles Data collection Pyxis planicauda Testudinidae Critically Endangered Trait data of endemic Madagascan plant species were com- piled from the literature, public databases (Madagascar Catalogue, ) and examination of herbarium specimens at the Royal Botanic Gardens, Kew (, specimens) and at epicarp (thin: , mm vs thick: $ mm), pulp type (i.e. fle- the Muséum National d’Histoire Naturelle, Paris ( speci- shy, non-fleshy (e.g. dry, spongy, sticky, fibrous, farinose) and mens). Traits recorded included life form (tree,
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