Can fruiting plants control animal behaviour and seed dispersal distance?

in Behaviour
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In an Afrotropical forest, we tested the hypothesis that fleshy-fruit plants with interspecific differences in fruit quality and quantity affect ranging behaviour of their seed dispersal vector. If fruiting plants could affect their dispersal vector, the plants also affect their seed dispersal distance and eventually their plant population biology. From 2007 to 2011, we measured seed transport by georeference daily bonobo group movements via GPS. Seed dispersal distance was estimated with mechanistic model, using 1200 georeferenced dispersal events and the average seed transit time through bonobo (24.00 h). We compared dissemination for eight plant species that deal with this trade-off: attracting dispersers by means of fruit quality/quantity versus retaining them in the patch because of the same quality/quantity value that attracted them. Because fruit traits of these eight species were different, we expected a difference in seed dispersal distance. Surprisingly, seed dispersal distances induced by bonobos were not affected by fruit traits. Although fruit nutrient contents, abundance and average patch feeding duration differed between plant species, patch feeding time was not related to subsequent dispersal distances. The apes’ dispersal distance survey gave an average dispersal distance estimated of 1332 ± 24 m from the parent plant (97.9% > 100 m). To conclude, feeding time invested in the patch, fruit quality and abundance had no apparent effect on bonobo seed dispersal distance. The possible effects in plant population biology are discussed.

Can fruiting plants control animal behaviour and seed dispersal distance?

in Behaviour



BeauneD. (2012). Latest news from the bonobos: Pan paniscus myths and realities. — Rev. Primatol. 4 DOI:10.4000/primatologie.1090.

BeauneD.BretagnolleF.BollacheL.HohmannG.SurbeckM.BoursonC.FruthB. (2013a). The bonobo–Dialium positive interactions: seed dispersal mutualism. — Am. J. Primatol. 75: 394-403.

BeauneD.BretagnolleF.BollacheL.HohmannG.SurbeckM.FruthB. (2013b). Seed dispersal strategies and the threat of defaunation in a Congo forest. — Biodiv. Conserv. 22: 225-238.

BeauneD.BretagnolleF.BollacheL.BoursonC.HohmannG.FruthB. (2013c). Ecological services performed by the bonobo (Pan paniscus): seed dispersal effectiveness in tropical forest. — J. Trop. Ecol. 29: 367-380.

BeauneD.FruthB.BollacheL.HohmannG.BretagnolleF. (2013d). Doom of the elephant-dependent trees in a Congo tropical forest. — Forest Ecol. Manage. 295: 109-117.

Campos-ArceizA.BlakeS. (2011). Megagardeners of the forest — the role of elephants in seed dispersal. — Acta Oecol. 37: 542-553.

CarloT.A.MoralesJ.M. (2008). Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. — J. Ecol. 96: 609-618.

ChapmanC.A.ChapmanL.J.WranghamR.HuntK.GeboD.GardnerL. (1992). Estimators of fruit abundance of tropical trees. — Biotropica 24: 527-531.

ClarkC.PoulsenJ.ParkerV. (2001). The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest. — Biotropica 33: 606-620.

ClarkC.PoulsenJ.BolkerB.ConnorE.ParkerV. (2005). Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. — Ecology 86: 2684-2694.

CôrtesM.C.UriarteM. (2012). Integrating frugivory and animal movement: a review of the evidence and implications for scaling seed dispersal. — Biol. Rev. 88: 226-254.

CousensR.D.HillJ.FrenchK.BishopI.D. (2010). Towards better prediction of seed dispersal by animals. — Funct. Ecol. 24: 1163-1170.

FlemingT.H. (1979). Do tropical frugivores compete for food?Am. Zool. 19: 1157-1172.

ForgetP.-M.JordanoP.LambertJ.E.Böhning-GaeseK.TravesetA.WrightS.J. (2011). Frugivores and seed dispersal (1985–2010); the ‘seeds’ dispersed, established and matured. — Acta Oecol. 37: 517-520.

FruthB.HohmannG. (1993). Ecological and behavioral aspects of nest building in wild bonobos (Pan paniscus). — Ethology 94: 113-126.

GardenerC.McIvorJ.JansenA. (1993). Passage of legume and grass seeds through the digestive tract of cattle and their survival in faeces. — J. Appl. Ecol. 30: 63-74.

HohmannG.FruthB. (2003). Lui Kotal – a new site for field research on bonobos in the Salonga National Park. — Pan Afr. News 10: 25-27.

HohmannG.FowlerA.SommerV.OrtmannS. (2006). Frugivory and gregariousness of Salonga bonobos and Gashaka chimpanzees: the influence of abundance and nutritional quality of fruit. — In: Feeding ecology in apes and other primates ( HohmannG.RobbinsM.BoeschC. eds). Cambridge University PressCambridge p.  123-159.

HohmannG.PottsK.N’GuessanA.FowlerA.MundryR.GanzhornJ.U.OrtmannS. (2010). Plant foods consumed by Pan: exploring the variation of nutritional ecology across Africa. — Am. J. Phys. Anthropol. 141: 476-485.

HoweH.F.MiritiM.N. (2004). When seed dispersal matters. — BioScience 54: 651-660.

IdaniG. (1986). Seed dispersal by pygmy chimpanzees (Pan paniscus): a preliminary report. — Primates 27: 441-447.

JordanoP. (1995). Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. — Am. Nat. 145: 163-191.

JordanoP.GarcíaC.GodoyJ.A.García-CastañoJ.L. (2007). Differential contribution of frugivores to complex seed dispersal patterns. — Proc. Natl. Acad. Sci. USA 104: 3278-3282.

KanoT.MulavwaM. (1984). Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. — In: The Pygmy chimpanzee: evolutionary biology and behavior ( SusmanR.L. ed.). Plenum PressNew York, NY p.  435.

LeightonM. (1993). Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. — Int. J. Primatol. 14: 257-313.

LenzJ.FiedlerW.CapranoT.FriedrichsW.GaeseB.H.WikelskiM.Böhning-GaeseK. (2010). Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. — Proc. Roy. Soc. Lond. B: Biol. Sci. 278: 2257-2264.

LeveyD.J.GrajalA. (1991). Evolutionary implications of fruit-processing limitations in cedar waxwings. — Am. Nat. 138: 171-189.

LevinS.A.Muller-LandauH.C.NathanR.ChaveJ. (2003). The ecology and evolution of seed dispersal: a theoretical perspective. — Annu. Rev. Ecol. Evol. Syst. 34: 575-604.

McConkeyK.R.ChiversD.J. (2007). Influence of gibbon ranging patterns on seed dispersal distance and deposition site in a Bornean forest. — J. Trop. Ecol. 23: 269.

Muller-LandauH.C. (2004). Interspecific and inter-site variation in wood specific gravity of tropical trees. — Biotropica 36: 20-32.

Muller-LandauH.C.WrightS.J.CalderónO.ConditR.HubbellS.P. (2008). Interspecific variation in primary seed dispersal in a tropical forest. — J. Ecol. 96: 653-667.

NathanR.Muller-LandauH.C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. — Trends Ecol. Evol. 15: 278-285.

PaineC.E.T.NordenN.ChaveJ.ForgetP.-M.FortunelC.DexterK.G.BaralotoC. (2012). Phylogenetic density dependence and environmental filtering predict seedling mortality in a tropical forest. — Ecol. Lett. 15: 34-41.

PoulsenJ.R.ClarkC.J.ConnorE.F.SmithT.B. (2002). Differential resource use by primates and hornbills: implications for seed dispersal. — Ecology 83: 228-240.

Réjou-MéchainM.FloresO.BourlandN.DoucetJ.-L.FétékéR.F.PasquierA.HardyO.J. (2011). Spatial aggregation of tropical trees at multiple spatial scales. — J. Ecol. 99: 1373-1381.

RussoS.E.PortnoyS.AugspurgerC.K. (2006). Incorporating animal behavior into seed dispersal models: implications for seed shadows. — Ecology 87: 3160-3174.

SchuppE.W.JordanoP.GomezJ.M. (2010). Seed dispersal effectiveness revisited: a conceptual review. — New Phytol. 188: 333-353.

SeidlerT.G.PlotkinJ.B. (2006). Seed dispersal and spatial pattern in tropical trees. — PLoS Biol. 4: e344.

SpiegelO.NathanR. (2007). Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. — Ecol. Lett. 10: 718-728.

ter SteegeH.PitmanN.C.A.PhillipsO.L.ChaveJ.SabatierD.DuqueA.MolinoJ.-F.PrevostM.-F.SpichigerR.CastellanosH.von HildebrandP.VasquezR. (2006). Continental-scale patterns of canopy tree composition and function across Amazonia. — Nature 443: 444-447.

TsujiY.MorimotoM.MatsubayashiK. (2010a). Effects of the physical characteristics of seeds on gastrointestinal passage time in captive Japanese macaques. — J. Zool. 280: 171-176.

TsujiY.YangozeneK.SakamakiT. (2010b). Estimation of seed dispersal distance by the bonobo, Pan paniscus, in a tropical forest in Democratic Republic of Congo. — J. Trop. Ecol. 26: 115-118.

WestcottD.A.BentrupperbaumerJ.BradfordM.G.McKeownA. (2005). Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. — Oecologia 146: 57-67.

WhiteF. (1988). Party composition and dynamics in Pan paniscus. — Int. J. Primatol. 9: 179-193.

WillsonM. (1993). Dispersal mode, seed shadows, and colonization patterns. — Plant Ecol. 107: 261-280.


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    An habituated and identified bonobo of the party (here Emil) is swallowing the fruits and seeds of Dialium sp. at LuiKotale, DRC. The party is geolocalised at this point and continuously during 24 h (with GPS track log, including at least Emil) for an estimation of this seed dispersal event. Photo by LKBP/David Beaune. This figure is published in colour in the online edition of this journal, which can be accessed via

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    Illustration of the mechanistic seed dispersal model with an example of seed transport (Gambeya lacourtiana). Identified bonobo feeding trees were georeferenced during group observations (2007–2011, LuiKotale, DRC) and bonobo group movement daily recorded (dark track log). Theoretical seed deposition site were determined by actual bonobo group position (dark track log) after 24.00 h, corresponding to the average transit time for seed through bonobo.

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    There is no correlation between feeding time spent by the bonobo group on the fruiting plant and the dispersal distance induced by the group after 24 h. For 22 fruiting species analysed as whole (N=278, r=0.07, p=0.2422) or other species as Dialium sp. (122, r=0.01, p=0.8572) or Cissus dinklagei (50, r=0.22, p=0.1178) at LuiKotale, DRC. This figure is published in colour in the online edition of this journal, which can be accessed via

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    Seed dispersal distribution induced by bonobo based on group movement behaviour (N=1200 dispersal events with all plant species at LuiKotale, DRC) and fixed bonobo transport duration (transit time = 24.00 h).

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    Seed dispersal distances induced by bonobo group for eight plant species (Cissus dinklagei (N=173), Dialium sp. (362), Gambeya lacourtiana (56), Grewia sp. (97), Pancovia laurentii (73), Placodiscus paniculatus (48), Polyalthia suaveolens (61), Treculia africana (21)) at LuiKotale, DRC.


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