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Characterization of Animal Communities Involved in Seed Accepted: 25 August 2017 DOI: 10.1111/aje.12480 ORIGINAL ARTICLE Characterization of animal communities involved in seed dispersal and predation of Guibourtia tessmannii (Harms) J.Leonard, a species newly listed on Appendix II of CITES Felicien Tosso1,2 | Gauthier Cherchye1 | Olivier J. Hardy2 | Kasso Da€ınou3 | Georges Lognay4 | Nikki Tagg5 | Barbara Haurez1,3 | Alain Souza6 | Stephanie Heuskin4 | Jean-Louis Doucet1 1TERRA Teaching and Research Centre, Central African Forests, Gembloux Agro-Bio Abstract Tech, University of Liege, Gembloux, Characterization of the ecology of endangered timber species is a crucial step in Belgium any forest management strategy. In this study, we described the animal communities 2Evolutionary Biology and Ecology Unit, CP 160/12, Faculte des Sciences, Universite involved in seed dispersal and predation of a high-value timber species Guibourtia Libre de Bruxelles, Brussels, Belgium tessmannii (Fabaceae; Detarioideae), which is newly listed on Appendix II of CITES. 3Nature+ asbl, Wavre, Belgium We compared the animal communities between two forest sites (Bambidie in Gabon 4Analytical Chemistry, Department Agro-Bio Chemistry, Gembloux Agro-Bio Tech, and Ma’an in Cameroon). A total of 101 hr of direct observations and 355 days of University of Liege, Gembloux, Belgium camera trapping revealed that a primate (Cercopithecus nictitans nictitans) and a 5Centre for Research and Conservation, Royal Zoological Society of Antwerp hornbill (Ceratogymna atrata) were important seed dispersers in Gabon. Conversely, (RZSA), Antwerp, Belgium a greater presence of a rodent (Cricetomys emini), which could act both as predator 6 Laboratoire de Physiologie Animale, and disperser, was observed in Cameroon. This study suggests that animal commu- Electrophysiologie et de Pharmacologie, Faculte des Sciences, Universite des nities involved in seed dispersal of G. tessmannii may vary depending on environ- Sciences et Techniques de Masuku, mental conditions and anthropogenic impacts. However, further studies are needed Franceville, Gabon to properly identify the factors involved in seed dispersal and predation of G. tess- Correspondence mannii. Felicien Tosso. Email: [email protected] Resume La description de l’ecologie des especes d’arbres en danger est une etape impor- Funding information ’ ^ Fonds pour la Formation a la Recherche tante pour toute strategie de gestion d une foret. Dans cette etude, nous avons dans l’Industrie et dans l’Agriculture, Grant/ decrit les communautes animales impliquees dans la dispersion et la consommation Award Number: FC1215 des graines d’une espece d’arbre de grande valeur, Guibourtia tessmannii (Fabaceae, Detarioideae), qui vient d’etre^ inscrite al’Annexe II de la CITES. Nous avons compare les communautes animales de deux sites forestiers (Bambidie, au Gabon, et Ma’an, au Cameroun). En tout, 101 heures d’observations directes et 355 jours de piegeage photographique ont rev el equ ’un primate (Cercopithecus nictitans nictitans)etun calao (Ceratogymna atrata) etaient d’importants disperseurs de graines au Gabon. Au Cameroun, par contre, nous avons constate une plus grande presence d’un rongeur (Cricetomys emini) qui peut agir comme disperseur et comme predateur. Cette etude suggere que les communautes animales impliquees dans la dispersion des semences de G. tessmannii peuvent varier selon les conditions environnementales et les impacts d’origine humaine. Cependant, de nouvelles etudes sont necessaires pour | Afr J Ecol. 2017;1–9. wileyonlinelibrary.com/journal/aje © 2017 John Wiley & Sons Ltd 1 2 | TOSSO ET AL. identifier correctement les facteurs impliques dans la dispersion et la predation des graines de G. tessmannii. KEYWORDS birds, Detarioideae, primates, seed dispersal, seed predation, tropical rainforest 1 | INTRODUCTION Hulme, 2005); rodents play a significant role in this process, for example through scatter hoarding (Forget & Vander Wall, 2001), A large proportion of plants depend upon animals for seed dispersal which is defined as a strategy when animals disperse seed reserves (Herrera and Pellmyr, 2009). In tropical forests, it has been estimated in small caches in many different locations (Brodin, 2010). that between 50% and 80% of tree species produce fruits that are The behaviour of seed dispersers can affect the genetically effec- dispersed by mammals and birds (Howe & Smallwood, 1982). Seed tive size of plant populations and the extent of gene flow between dispersal is a critical step in the biological cycle of plants and a key populations. Identifying the vectors involved in both primary and process for the maintenance of tropical forest biodiversity at differ- secondary seed dispersal processes might provide essential and prac- ent scales (Wang & Smith, 2002). tical information for forest management (Da€ınou et al., 2012). At a large scale, the composition and behaviour of dispersal agents Guibourtia tessmannii (Harms) J.Leonard is an important African may vary both geographically and temporally (Gautier-Hion, Gautier, & tree species, newly listed on Appendix II of CITES (Koumba Pambo Maisels, 1993). These variations might be due to (i) tight co-evolution- et al., 2016). Known as “bubinga” or “kevazingo, ” it has high commer- ary relationships between plants and seed dispersers (Chapman, Chap- cial and social importance and is currently under significant threat due man, & Wrangham, 1992) and (ii) plant community structure and to illegal logging (Tosso, Da€ınou, Hardy, Sinsin, & Doucet, 2015). Its composition (Dennis, 2007). The latter is influenced both by control- seeds are surrounded by a red aril, a typical characteristic of seeds pri- ling factors (e.g., climate and geologic materials) and by dependent fac- marily dispersed by primates and large birds (Gautier-Hion et al., tors (vegetation, consumers, decomposers and transformers, soil and 1985). However, knowledge regarding its ecology and more precisely microclimate) (Lewis, 1969). Anthropogenic pressures can also have a its dispersal and regeneration is lacking. The aim of this study was to significant influence: for example, land conversion and defaunation characterize the community of consumers of G. tessmannii fruits and caused by hunting modify the disperser community (Cordeiro & Howe, seeds in contrasting environmental conditions. 2003). In Africa, Effiom, Birkhofer, Smith, and Olsson (2014) showed that hunting pressure might have a local direct negative effect on large 2 | MATERIALS AND METHODS mammals and in turn may have direct and indirect effects on other trophic levels. It is therefore crucial to investigate seed dispersers of a 2.1 | Study species particular plant species across various habitats (Blake et al., 2012). The seeds and fruits produced by forest tree species contain Guibourtia tessmannii (Fabaceae; Detarioideae) is a large tree reach- important nutrients for frugivore and granivore communities (Guin- ing 40 m in height (Doucet, 2003) distributed in rainforests from don, 1997; Whitney et al., 1998). Moreover, seed and fruit traits, Cameroon to Gabon (Tosso et al., 2015). Guibourtia tessmannii is her- such as size and shape, influence these plant–animal interactions maphrodite and polyploid (Tosso et al., 2016). Its fruit is a pod (mean (Gautier-Hion et al., 1985; Rodrıguez, Alquezar, & Pena,~ 2013; Van- size Æ standard deviation: 3.32 Æ 0.65 cm long and 2.23 Æ 0.59 cm der Wall, 1990). The digestion processes as well as animal size also wide) which contains a single grain (mean size Æ standard deviation: play crucial roles (Stiles, 2000). There is thus a strong relationship 2.3 Æ 0.14 cm long and 1.15 Æ 0.21 cm wide) covered by a red aril, between fruiting plant species and their dispersal agents that can and its fruiting period extends from December to March (Meunier, affect both plant and animal communities in a forest ecosystem Moumbogou, & Doucet, 2015; Tosso et al., 2016). The species is (Cordeiro & Howe, 2003; Santos & Tellerıa, 1994). classified as nonpioneer light demanding (Doucet, 2003). Commer- As well as the relationships between fruiting plant species and cially known as bubinga or kevazingo, the wood has a very high their dispersal agents, the mechanisms of seed dispersal are also commercial value; in addition, its bark is used by local communities complex, in that many biotic processes—such as predation, pathogen for its medicinal properties (Tosso et al., 2015). attack and secondary dispersal—can affect the fate of seeds between primary dispersal and germination (Andresen et al., 2005). 2.2 | Study area Primary dispersal is the removal of a fruit from a tree and the depo- sition of its seeds in an establishment area (Stoner & Henry, 2009). The study was carried out in two evergreen forest concessions, both Secondary dispersal is defined as any significant movement of seeds managed by Forest Stewardship Council (FSC)-certified logging com- after primary dispersal from plants (Vander Wall, Forget, Lambert, & panies. The two sites exhibit quite different environmental TOSSO ET AL. | 3 conditions. “Wijma” concession (Cameroon) is located at Ma’an by villages, and the bushmeat trade is developed towards Equatorial (2°300N, 10°300E) (Figure 1a); the forest is dominated by Fabaceae- Guinea, whereas in Precious woods, human density is low and hunt- Cesalpinio€ıdeae (36.67%), Meliaceae (13.33%), Sapotaceae (13.33%) ing activities are poorly developed (Haurez, 2015). and Sterculiaceae (5%) (Table 1). The climate is equatorial (1 686 mm of annual rainfall and an annual average
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