Introduction
The conservation of a species is dependent upon the conservation of those species that provide it with ecological services. The question of how the extinction of one species could affect others is particularly pertinent in the case of the great apes (Hominidae: chimpanzee Pan troglodytes, bonobo Pan paniscus, gorilla Gorilla gorilla and orang-utan Pongo pygmaeus) because they play an important role as key dispersers of woody species (Wrangham et al., Reference Wrangham, Chapman and Chapman1994; Voysey et al., Reference Voysey, McDonald, Rogers, Tutin and Parnell1999; Gross-Camp & Kaplin, Reference Gross-Camp and Kaplin2011; Beaune et al., Reference Beaune, Bollache, Muganza, Bretagnolle, Hohmann and Fruth2013a,Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruthb,Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck and Fruthc; Effiom et al., Reference Effiom, Nuñez-Iturri, Smith, Ottosson and Olsson2013). This can also be extended to the lesser apes, the gibbons (Hylobatidae; McConkey & Chivers, Reference McConkey and Chivers2007). The bonobo was the last of the three African great ape species to be discovered. It is endemic to the Democratic Republic of Congo, south of the Congo River, and its habitat does not overlap with that of either chimpanzees or gorillas. Bonobos are mainly frugivorous (66% of feeding sessions), spending c. 3.5 hours per day swallowing seeds (Plate 1), which they transport over a relatively long distance (93% > 100 m; mean 1.2 km). An individual will disperse 9.1 t of seeds (11.6 million seeds > 2 mm in length, excluding those such as Ficus spp. and Musanga cecropioides) in its lifetime (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b). More than 91 plant species are dispersed by bonobos through endozoochory (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b). Passed seeds germinate more rapidly, more successfully and with greater post-dispersal survival than unpassed seeds (seeds embedded in faeces are involved in diplochory with dung beetles; Beaune et al., Reference Beaune, Bollache, Bretagnolle and Fruth2012a). In the forest of LuiKotale 40% of tree species and 65% of individual trees rely on bonobos for seed dispersal, and functional overlap between the bonobo and other frugivorous animals appears to be low (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b,Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck and Fruthc).
Plate 1 Bonobo Pan paniscus eating velvet tamarind fruits (Dialium sp.) and swallowing seeds at LuiKotale, Democratic Republic of Congo. Photograph: David Beaune/LKBP.
The seed dispersal service provided by bonobos is of particular interest as the species is categorized as Endangered on the IUCN Red List (Fruth et al., Reference Fruth, Benishay, Bila-Isia, Coxe, Dupain and Furuichi2008), listed on CITES Appendix I (CITES, 2014) and under Class A in the African Convention on the Conservation of Nature and Natural Resources (OAU, 2010). The population is estimated to number 29,500–50,000 (Fruth et al., Reference Fruth, Benishay, Bila-Isia, Coxe, Dupain and Furuichi2008). The greatest threat to the bonobo is poaching for the commercial bushmeat trade but the species’ survival is also threatened by forest fragmentation and degradation. Despite international protection and local taboos bonobos are still killed in their natural habitats, including in protected areas such as Salonga National Park (Hart et al., Reference Hart, Grossmann, Vosper, Ilanga, Furuichi and Thompson2008).
I assessed the ecological importance of bonobos for fruiting plants by investigating the ability of the plant community to recruit without horizontal seed dispersal (i.e. without bonobos and other seed dispersal vectors). The hypothesis is that without seed dispersal several plant species for which apes are obligate seed dispersers would not recruit under the parental tree because of density-dependent effects on the survival of seeds and seedlings. I also discuss how bonobos depend on trees in this plant–animal mutualism.
Study site
Fieldwork took place at LuiKotale, at the south-western fringe of Salonga National Park, Democratic Republic of Congo (Fig. 1). The study site comprised > 100 km2 of primary evergreen lowland tropical rain forest (for more information about the study site and previous research conducted there see Beaune et al., Reference Beaune, Bollache, Bretagnolle and Fruth2012a,Reference Beaune, Bollache, Fruth and Bretagnolleb,Reference Beaune, Bollache, Fruth, Hohmann and Bretagnollec, Reference Beaune, Bollache, Muganza, Bretagnolle, Hohmann and Fruth2013a,Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruthb,Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck and Fruthc,Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck, Bourson and Fruthd,Reference Beaune, Fruth, Bollache, Hohmann and Bretagnollee).
Fig. 1 Location of the study site at LuiKotale, in Salonga National Park, Democratic Republic of Congo.
Methods
To assess seedling recruitment under the parent crown, mature trees of 22 species previously observed to fruit (thus excluding males of dioecious species) and efficiently dispersed by bonobos (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b) were investigated during May 2010–June 2011, following the methodology of Chapman & Chapman (Reference Chapman and Chapman1995). All seedlings (< 50 cm high), saplings (50–200 cm high) and poles (> 200 cm high, < 10 cm diameter at breast height, DBH) were censused in the parental crown area (i.e. the fruit-fall zone) of adult trees >10 cm DBH, with no conspecifics within 10 m of the fruit-fall zone. The presence of seeds under the parental crown was confirmed by observation of falling seeds during animal feeding sessions and/or visual assessment of seeds present (fragments and fresh seeds). Mean numbers of seedlings, saplings and poles were calculated from a minimum of five adult plants per species. We considered an adult plant to be able to self-replace when the mean pole production per plant was ≥ 1. To confirm that a species was able to recruit outside its fruit-fall zone, density of recruits was estimated across the total census area.
Results
Nineteen plant species (three liana and 16 tree species) were dispersed efficiently by bonobo (Table 1). Three species considered to be autochorous (i.e. dispersed by a plant's own means) were included in the assessment for comparison (see Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b,Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck and Fruthc for characterization of seed dispersal). For each plant species some seeds were not dispersed horizontally and were found under the parental crown. During bonobo and monkey (Cercopithecus cephus ascanius, Cercopithecus mona wolfi, Lophocebus aterrimus) feeding sessions broken branches and fruits with seeds (dropped or spat) from the 19 fruiting plants were observed on the ground. The autochorous species recruited, on average, more than one pole under the parents, thus fulfilling the criterion for self-replacement. In contrast, the fleshy-fruited species dispersed by bonobos did not recruit enough poles under parent plants for self-replacement, except for Drypetes sp. (Table 1, Fig. 2). Although seedlings, saplings and poles were found under other tree species (in a total of 5.13 ha censused), most adults of zoochorous (i.e. dispersed by animals) species were not able to self-replace without seed dispersal beyond the fruit-fall zone, despite the presence of a seed bank.
Fig. 2 Mean (±SE) recruitment of poles (< 10 cm DBH) under the parent crown for three autochorous species (HM, Hymenostegia mundungu; ScZ, Scorodophloeus zenkeri; StZ, Strombosiopsis zenkeri) and 19 species dispersed by bonobos Pan paniscus (AM, Anonidium mannii; BW, Blighia welwitschii; CS, Canarium schweinfurthii; CD, Cissus dinklagei; DS, Drypetes sp.; EO, Enantia olivacea; FS, Ficus sp.; GL, Gambeya lacourtiana; GO, Grewia oligoneura; GS, Greenwayodendron suaveolens; IG, Irvingia gabonensis; IGr, Irvingia grandifolia; KG, Klainedoxa gabonensis; LF, Landolphia forestiana; LS, Landolphia sp.; MA, Mammea africana; MY, Manilkara yangambiensis; PL, Pancovia laurentii; PE, Parinari excelsa) at LuiKotale (Fig. 1). The dotted line is the threshold for self-replacement of the parent.
Table 1 Mean number of seedlings, saplings and poles found under the canopy of adult individuals of 22 tree and liana species in LuiKotale, Democratic Republic of Congo (Fig. 1).
1 Botanical nomenclature follows the African Plants Database v. 3.4.0 (2014)
2 The limiting greatest seed width or digestive tract passage size, indicated as diameter (ø) or length (↔)
Discussion
The frugivorous bonobo relies on the fruits of 107 plant species, which account for > 55% of their diet (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Bourson, Hohmann and Fruth2013b). During certain months trees such as Dialium spp. can account for > 82% of the bonobo's diet (Beaune et al., Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck, Bourson and Fruth2013d). How tree populations depend on the ecological services provided by bonobos is more difficult to assess.
However, without seed dispersal, zoochoric plant species normally dispersed by bonobo recruit insufficient young under the fruit-fall zone for self-replacement, despite regular seed restocking by gravity (barochory without zoochory/anemochory). This may be attributable to the incapacity of seeds to germinate without handling and/or to higher mortality under the parental crown as a result of density-dependent effects (Janzen, Reference Janzen1970; Connell, Reference Connell, Boer and Gradwell1971; Schupp, Reference Schupp1992; Beaune et al., Reference Beaune, Bollache, Fruth, Hohmann and Bretagnolle2012c, Reference Beaune, Bollache, Muganza, Bretagnolle, Hohmann and Fruth2013a). Bush pigs Potamochoerus porcus, giant pouched rats Cricetomys emini and 17 other seed predators at LuiKotale were observed foraging seeds under parent plants, and reduced seed survival under the parental canopy (Beaune et al., Reference Beaune, Bollache, Bretagnolle and Fruth2012a,Reference Beaune, Bollache, Fruth and Bretagnolleb, Reference Beaune, Bretagnolle, Bollache, Hohmann, Surbeck and Fruth2013c). Herbivorous animals also reduced the survival of seedlings, saplings and poles, in a density-dependent effect occurring under the parent plant, where a higher density of seeds attracts more predators. An alternative way of examining this would be to compare two botanical plots from the same forest block, with and without bonobo populations, or the same plot with a before and after control impact assessment after bonobo extinction. However, this would pose ethical and logistical problems. Despite its limitations the assessment presented here gives an indication of the seed and recruitment mortality under the parental crown of species adapted to zoochory. Other, smaller seed dispersal vectors, such as monkeys, bats and birds, could fulfil the seed dispersal role of the apes for certain fruiting plants, but less effectively because the seed handling process, the dispersal distance, the number of seeds disseminated, and the secondary dispersal by dung beetles would not be equivalent. Without the bonobo more seeds would fall in the fruit-fall zone, increasing the seed bank and consequently seed mortality as a result of increased predation. A similar survey for elephant-dispersed plant species in the absence of elephants yielded the same result: the trees did not recruit sufficiently for self-replacement, and seed predation was not saturated (Beaune et al., Reference Beaune, Fruth, Bollache, Hohmann and Bretagnolle2013e). Fruiting plants, especially species with small seeds and several dispersal vectors, could potentially survive an extinction of the bonobo, but this needs to be investigated further. The seed dispersal service provided by bonobos could be provided by other, smaller animals but without the same dispersal effectiveness (and with potential population genetics effects on the plants). Unlike the bonobo-dispersed species, autochoric trees such as Hymenostegia mundungu, Scorodophloeus zenkeri and Strombosiopsis zenkeri are adapted to short dispersal distance and their seeds probably contain antifeedant and other toxic compounds.
Preserving protected areas from deforestation but not from poaching can lead to the so-called empty forest syndrome (Redford, Reference Redford1992). With bushmeat trafficking affecting apes and other dispersal vectors in many forests (Bowen-Jones & Pendry, Reference Bowen-Jones and Pendry1999; Fa et al., Reference Fa, Ryan and Bell2005; Nuñez-Iturri & Howe, Reference Nuñez-Iturri and Howe2007; Wright et al., Reference Wright, Hernandéz and Condit2007; Brodie et al., Reference Brodie, Helmy, Brockelman and Maron2009; Vanthomme et al., Reference Vanthomme, Bellé and Forget2010; Effiom et al., Reference Effiom, Nuñez-Iturri, Smith, Ottosson and Olsson2013), apparently healthy adult tree populations may be threatened with extinction. Is the future of the tropical forest one of ecosystem simplification favouring autochoric and anemochoric species? Conservation strategies for apes need to include tree conservation, just as conservation of trees and other fruiting plants must include conservation of apes and other seed-dispersal vectors.
Acknowledgements
I thank the Institut Congolais pour la Conservation de la Nature for granting permission to conduct research at Salonga National Park, and the people of Lompole for granting permission to access the forest of their ancestors. Research at LuiKotale was conducted under the auspices and with the financial support of the Max Planck Society, the German Ministry of Education and Research, le conseil régional de Bourgogne, and the SFE and SFDP (France). I thank the international and local staff of LuiKotale, Gottfried Hohmann, Barbara Fruth, Loïc Bollache and François Bretagnolle for their support.
Biographical sketch
David Beaune specializes in conservation and ecological services. His interests cover various ecosystems and species, from the poles to the equator. He is working to establish a scientific organization to facilitate a positive anthropogenic effect on the environment.
