Role of the western lowland gorilla (Gorilla gorilla ... et al_author...Role of the western lowland gorilla (Gorilla gorilla ... ... 3, 3

BASE Biotechnol. Agron. Soc. Environ.201317(3),517-526 Focus on:

Roleofthewesternlowlandgorilla(Gorilla gorilla gorilla)inseeddispersalintropicalforestsandimplicationsofitsdeclineCharles-AlbertPetre(1,2,3),NikkiTagg(3),BarbaraHaurez(1),RoselineBeudels-Jamar(2),Marie-ClaudeHuynen(4),Jean-LouisDoucet(1)(1)Univ.Liege-GemblouxAgro-BioTech.LaboratoryofTropicalandSubtropicalForestry.UnitofForestandNatureManagement.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:[email protected](2)RoyalBelgianInstituteofNaturalSciences.ConservationBiologyUnit.RueVautier,29.B-1000Brussels(Belgium).(3)RoyalZoologicalSocietyofAntwerp.CentreforResearchandConservation.ProjetGrandsSingesCameroon.KoninginAstridplein,20-26.B-2018Antwerpen(Belgium).(4)Univ.Liege.DepartementofBiology,EcologyandEvolution/BehavioralBiology-EthologyandAnimalPsychology.QuaiVanBeneden,22.B-4020Liege(Belgium).

ReceivedonSeptember17,2012;acceptedonMay8,2013.

Patternsofseeddispersalsignificantlyaffectplantdemography,dynamicsandsuccession.Inthetropics,themajorityoftreespeciesbearfruits thatareadapted toanimal-mediateddispersal.Amongstseeddispersers, thecontributionofprimates iswidelyrecognizedbyecologistsasincomparable.However,inlowlandAfrotropicalforests,thespecificroleofthelargestprimatespecies,thewesternlowlandgorilla(Gorilla gorilla gorillaSavageandWyman,1847),hasbeenoverlooked.Thisisofparticularrelevanceasthisspeciesseemstofulfillimportantcriteriaforeffectivedispersal,bothquantitativelyandqualitatively.Onetraitmakesitpotentiallyuniqueasseeddisperser;theregulardepositionofseedsinopencanopyenvironmentswherelightwillnotbealimitingfactorforsubsequentseedlinggrowthandsurvival.Themagnitudeofwhichthisparticulartraitcontributestoforestdynamicsremainsunexploredthoughitcouldbepotentiallyimportant.Itmightnolongerbethecase,however,asthewesternlowlandgorillaiscriticallyendangered.Thelossoftheecologicalservicesprovidedbylarge-bodiedseeddispersersmayhaveconsiderableimpactsontheforests.Throughdispersallimitation,populationdynamicsofplantsinforestsdevoidoflargefrugivoreswillbestronglyimpacted.Inthelong-term,thismayleadtoshiftsinplantcommunitystructure,compositionandtoreducedtreediversity.Currently,forestsoftheCongobasinfaceincreasinglevelofdeforestationanddegradation,whichputsalready theecosystem integrity in jeopardy.Theadditional threat that represents frugivorouswildlifedepletionisthereforeofforestmanagementconcern.Keywords.Seeddispersal,primate,forestdynamics,Africa.

Le rôle du gorille des plaines de l’Ouest (Gorilla gorilla gorilla) dans la dissémination des graines en forêts tropicales et les implications de son déclin. Ladisséminationdesgrainesparlesanimauxparticipesignificativementàladémographie,ladynamiqueetlasuccessiondescommunautésvégétales.Enforêtstropicales,lamajoritédesarbresproduisentdesfruitsadaptésàlaconsommationetàladisséminationdeleursgrainesparlesanimaux.Parmilesdifférentsagentsdisséminateurs,lesprimatesjouentunrôleinégalable,largementreconnu.Alorsqueleurrôlefondamentaldanslarégénérationforestièreetlemaintiendelabiodiversitétropicaleestaccepté,lacontributionspécifiquedugorilledesplainesdel’Ouest(Gorilla gorilla gorillaSavageandWyman,1847),leplusgranddesprimatesdesforêtsduBassinduCongo,resteméconnue.Pourtant,cetteespècesembleréunirlesconditionsfondamentalespourqu’unedisséminationtrèsefficaceseréalise.Ilsedistinguenotammentpar unedispersion régulière des graines dans desmicro-habitats caractérisés par une forte ouverture de la canopéeoù lalumièreneserapasunfacteurlimitantàlacroissanceetlasurviedesjeunesplants.L’influencesurladynamiqueforestièrequepourraitjouercetenrichissementengrainesdanslesouverturesforestièresparlegorilledesplainesdel’Ouestn’apasencoreétéexploréemalgrésonimportancepotentielle.Ellepourraitcependantneplusêtreactivecomptetenudesmenacescritiquesquipèsentsurlasurviedespopulationsdegorilles.Lapertedesservicesécologiquesrendusparlagrandefaunedisséminatricedegrainespourraitavoirdesconséquencesconsidérablessurlefuturdesforêts.Enl’absencededissémination,ladynamiquedepopulationdenombreuses espèces serait impactée.Sur le long terme, cela pourrait conduire à unemodificationde la

518 Biotechnol. Agron. Soc. Environ. 201317(3),517-526 PetreC.-A.,TaggN.,HaurezB.etal.

1. INTRODUCTION

Plants bearing fleshy fruits are believed to have amutualistic relationshipwith theiranimalconsumers:fromanevolutionaryperspective,plantstakeadvantageof seed dispersal while animals benefit from thenutritivevalueoftheconsumedfruit(Kollmann,2000).Frugivore-mediated seed dispersal (i.e. zoochory)can have significant effects on plant demography,dynamics, succession and spatial distribution at allscale (Kollmann, 2000; Seidler et al., 2006; Blakeetal.,2009;Gillespieetal.,2012).

In the tropics, the majority of tree species bearfruits adapted to animal dispersal. In Neotropicalforests, Howe et al. (1982) reported the proportionof animal-dispersed species ranging from51 to 93%forcanopytreesand77to98%forsub-canopytrees.InPaleotropicalforests,treesalsoexhibitadaptationsfor animal seed dispersal. According to Doucet(2003), about 60% of tree species of CentralGabonare dispersed through endozoochory, and in the Djaregion,South-EastCameroon,thisvaluereaches82%(Letouzey, 1985). Despite the importance of seeddispersal in biodiversitymaintenance (Janzen, 1970;Connell, 1971; Harms et al., 2000; Hardesty et al.,2006), mechanisms affecting seed dispersal patternsand recruitment probability of tropical trees remainpoorly documented. Furthermore, no generalizationintending to predict these parameters for less-knowntreespeciesispossibleduetothecomplexityoftropicalecosystems(Müller-Landauetal.,2008).

Fruitsandseedsadaptedtozoochoryvarywidelyin their shape, size, color, chemical composition,palatability, digestibility and accessibility; thereforethey attract and are dispersed by different sets ofanimal species (Poulsen et al., 2002;Müller-Landauet al., 2008). Behavioral and physiological patternsof frugivorous dispersers, such as activity budget,displacement velocity and distance, retention timeand fruit handling, will have consequences on seedviabilityandspatialpatternsofseeddeposition(Howeet al., 1982; Lambert et al., 1998; Traveset, 1998;Nathan etal., 2008); factors which greatly influencerecruitment probability. Seed dispersal, populationdynamicsandcommunitystructureatagivensitearethus dependent on the frugivorous community andplantattributesthatattractthem.

As primates represent a great proportion of thefrugivorousbiomassintropicalforests(Garberetal.,1998), in general their contribution to seed dispersalhasreceivedmuchattentionandtheyarebelieved,asagroup,tobeincomparabledispersers(Poulsenetal.,2001;Lambert,2011).Thatsaid,forsomefrugivorousprimate species, documentation of their role as seeddisperserislacking,despitetheirpotentialeffectiveness.If such potentially effective dispersers disappearfrom forests, there could be long-term detrimentalconsequences for natural forest regeneration anddynamics (Terborgh et al., 2008; Blake et al., 2009;Poulsen, 2009;Vanthomme et al., 2010). The futureoftropicalforestsisalreadyputinjeopardybyhumanactivities imposing immediate effects on its size,structure and composition, and climate change willfurthercontribute to this (Wright,2010;deWasseigeetal., 2012). Extirpation of effective dispersersconstitutes another major threat for the forests thatwillremain.Thismaybethecasewiththe“criticallyendangered”western lowlandgorilla (Gorilla gorillagorillaSavageandWyman,1847)(IUCN,2012).

Here, we investigate the potential importanceandeffectivenessofwestern lowlandgorillasasseeddispersers and scrutinize the potential consequencesof their removal/extinction for the preservation ofthe ecosystem integrity. Specifically, the objectivesofthisreviewarethreefold.First,weaimtodescribetheadvantagesandunderlyingmechanismsofanimal-mediated seed dispersal for plant fitness in tropicalecosystems.Wethenexplaintheimportantecologicalfunction of primates as a seed dispersal taxon, wesummarizewhatweknowaboutthecontributionofthewestern lowlandgorillaandmakeexpectationsof itseffectiveness.Finally,wediscussthekeystoneroleoflarge frugivores and the implicationsof their declineforthefutureoftropicalforests.

For the purpose of this review of the literatureweused thedatabaseScopusprovidedbyGemblouxAgro-Bio Tech. The main keywords entered were“seeddispersal”,“westernlowlandgorilla”,“primate”,“endozoochory”, “tropical forest”, “regeneration”,“forest degradation” and “Congo Basin”. Amongrelevant references, the most recent were selected,withtheexceptionofpublicationsdefiningecologicalconcepts,andillustrationsfromCentralAfricanforestswereprioritized.

structureetcompositiondelacommunautévégétaleetàunappauvrissementdeladiversité.Actuellement,lesforêtsdubassinduCongosubissentdestauxgrandissantsdedéforestationetdégradationquimettentenpérill’intégritédel’écosystème.Ladisparitiondesfrugivoresconstituedoncunemenaceadditionnellequidoitêtrepriseenconsidérationdanslagestiondesmassifsforestiers.Mots-clés.Disséminationdesgraines,primate,dynamiqueforestière,Afrique.

Westernlowlandgorillaseeddispersal 519

2. ENDOZOOCHORY: ADVANTAGES AND DISADVANTAGES

Seed dispersal, regardless of the type of vector, isbelieved to confer an advantage to theplant throughdifferent mechanisms, which increase recruitmentprobability. It reduces the mortality rate caused bysiblingcompetition(Connell,1971),intensepredationby granivores and grazers that concentrate theiractivities where food is abundant (Janzen, 1970),and attacks by specific pathogens (Augspurger,1984).Escape fromadensity- or distance-dependentmortality is described by the “Escape Hypothesis”,betterknownastheJanzen-Connellhypothesis(Howeetal.,1982).Seeddispersalalsoenablescolonizationof particular habitats that are unpredictable in whentheywillbecreatedorintheirlocation,suchastreefallgaps(Howeetal.,1982).Thisadvantageisexplainedby the “ColonizingHypothesis”. In the specific caseofendozoochory,theextracostsinvolvedinproducingfruits to attract animals is associatedwith additionalevolutionary advantages, known as the “Directed-DispersalHypothesis”.Thishypothesisconsidersthatnon-randommovementandhabitatpreferenceofsomefrugivores results in a disproportionate deposition ofseeds in sites where specific requirements for seedgerminationandseedlinggrowthandsurvivalaremet(Howeet al., 1982;Wenny,2001).This evolutionofplanttraitshasfurtherconsequencesthatmayimprovethe fate of dispersed seeds; passage through the gutofafrugivoreisnormallyassociatedwithmechanicalandchemicalabrasionoftheseedcoatwhich,insomecases,impactspositivelyongerminationcapacity(e.g.,Liebermanetal.,1986;Traveset,1998;Valentaetal.,2009). Furthermore, when excreted, these seeds aresurroundedby fecalmaterial thatprotects themfromhydric stress and offers a nutrient-rich environmentthatencouragesseedlinggrowthandincreasessurvivalprobability(Nchanjietal.,2003).Finally,dungbeetlesare attracted to volatile organic compounds emittedfromfecesandinitiatesecondarydispersalwhichcanhaveahuge impactonseedsurvival,seedpredation,germination success and seedling establishment(Shepherdetal.,1998;Andresenetal.,2004).

Despite the numerous potential advantages ofendozoochory, attracting frugivores through fruitproduction is, however, no guarantee for increasedplantfitnessthroughhigherrecruitmentsuccess.Somefrugivoresdonotdispersetheseedsfromsomeorallspeciestheyfeedon,theymaybreaktheseedsandkilltheembryowhenmouth-processingorevenmasticatetheseedsonpurposefornutrient intake(Tutinetal.,1993;Lambertetal.,1998).Thisresultsinthembeingseedpredators instead.Passage through thegut doesnot always enhance germination success or rate ofallof thefruit itemsconsumed(Traveset,1998).The

level of abrasion of the seed coat and its effect ongerminationdependsontheconsumerspeciesandtheintrinsiccharacteristicsofseeds,suchasthicknessandhardnessoftheseedcoat,aswellasseedsize,whichaffectstheguttransittime;smallerseedsareretainedfor longer periods than larger ones (Traveset, 1998).A long retention time can enhance germination rateandsuccessthroughsuppressingseeddormancyorbysofteningtheseedcoatandincreasingitspermeability.However, a retention time that is too long can leadin some cases to total seed digestion or germinationinhibition (Lieberman et al., 1986; Traveset, 1998).Additionally, the chemical compounds in the feces(e.g. fatty acids and phenols) can sometimes act asgermination inhibitors (Valenta et al., 2009) andfecal material can reduce germination success byfacilitatingfungalandbacterialdevelopment(Travesetetal.,2007).Similarly,thefruitpulpmayalsocontaingerminationinhibitors(Robertsonetal.,2006)andthepresenceofpulpsurroundingtheseedsalsoincreasestheriskoffungalandbacterialdevelopment thatcanbe lethal to seeds (Baskin et al., 1998). Therefore,undispersed seeds still surrounded by the fruit pulp,either due to dispersal failure (lack of dispersers’visitation) or as a result of seed processing behavior(spittingofseedsnotclearedfrompulp),arelikelytoface a highmortality rate. Furthermore, dung beetleactivity can result in seed loss, by excessively deepburialinthesoil(Shepherdetal.,1998).Finally,theseed deposition pattern exhibited by large frugivoresresults in a high density of seeds per fecal clumpwhich,toacertainextent,cancelsouttheadvantageofescapingfromdensity-dependentmortalityunderneaththecrownoftheparent(Poulsenetal.,2001;Travesetetal.,2007).

Production of fruit attributes that attract animalsrepresents an energy investment by the plant, whichwouldnotbecosteffectiveincaseofdispersalfailureinhabitatswhereanimaldispersersarereducedtoverylowdensities or are locally extinct. In general, fruit-bearingplantswouldhavemultipleanimaldispersers,especially in tropical forests where the frugivorecommunity is highly diverse (Müller-Landau et al.,2008). However, some plants rely on a limited setof dispersers or even a single species and thereforehave restricted or no dispersal substitution capacity(Liebermanetal.,1986;Tutinetal.,1991a;Babweteeraet al., 2007; Blake et al., 2009). Local extinction ofdispersers could therefore lead to important plantpopulation decline through recruitment limitation(Terborghetal.,2008).

In the tropics, strict one-to-one plant-animalmutualisms occurmainly due to size restriction: bigseedscanonlybedispersedbylarge-bodiedfrugivoreswithacorrespondinglylargegutsize(Babweteeraetal.,2007).TheAfricanforestelephant(Loxodonta cyclotis


Matschie,1900) is the largest forestdwellinganimalonEarthandithasbeenreportedtobetheexclusivedisperser of at least 13tree species atNdoki Forest,RepublicofCongo(Blakeetal.,2009).Similarly,thewesternlowlandgorillaistheonlyregulardisperserofseedsofCola lizaeN.Hallé (Sterculiaceae), endemicto central Gabon, despite the fact that sympatricchimpanzeesoccasionallyswallowanddisperse theirseeds (Tutin et al., 1991a). Crucially, both species,westernlowlandgorillasandAfricanforestelephants,are currently facing considerable population declinethroughouttheirrange(IUCN,2012).

3. PRIMATES AS A KEYSTONE TAXON FOR TROPICAL FORESTS

3.1. Importance of primates as a seed disperser group: generalities

Amonganimalseeddispersersintropicalecosystems,the contribution of primates is thought to be ofparamountimportance(Poulsenetal.,2001;Lambert,2011). Primates are usually abundant and have arelatively large body size. As most primate specieshave a high frugivorous diet, they represent alarge proportion of the frugivores biomass and areconsequently responsible for the removal of a largeproportionofthefruitandseedcrop(Chapman,1989;Chapmanetal.,1998;Garberetal.,1998;Poulsenetal.,2002; Lambert, 2011). In such cases, diet overlap iscommon(e.g.Chapman,1989;Tutinetal.,1993;Tutinetal.,1994;Poulsenetal.,2001;Poulsenetal.,2002;Lambert,2011),resultinginsomedegreeofredundancyamong primates in the seed dispersal service forvariousplantspecies.Multi-speciesdispersalofseedshasagreatinfluenceontheseedshadowoftheplantsconcerned(i.e.,thespatialdistributionofseedsaroundtheparental source;Willson,1993)andsubsequentlyon recruitment probability. Indeed, primates withina community exhibit a variety of feeding strategies,differences in fruit and seed processing, home rangesize, habitat preference, daily travel distance, gutcapacity and retention time of the digesta (Poulsenetal.,2001).Asaresult,distinctprimatespecieswilldisperse seeds intodifferenthabitat types, atvaryingdistances from the parent plant, and according to ascattered or rather clumped distribution pattern. Theprobability of encountering suitable conditions forrecruitmentisthereforehigherincaseofmulti-speciesseeddispersal(Poulsenetal.,2001).

Contrary to this, some sympatric primate speciesexhibit diet specialization for certain fruit species,which increases the proportion of seed species in aplant community that is dispersed. For instance, thenumberofseedspeciesdispersedbyeachfrugivorous

primate species in a study site in theDjaBiosphereReserve,Cameroon,wasfoundtorangefrom5to61,whereasasawholetheprimatecommunitydispersedat least125seedspecies throughfecalclumps;77ofthembeingtreespecies,whichrepresented34%ofthestudiedtreefloraofthereserve(Poulsenetal.,2001).

These varying dietary, behavioral and ecologicalcharacteristics result in a primate community that isdiverse yet effective at seed dispersal and thereforeabletosignificantlystructurethehabitatsinwhichtheyarefound(Poulsenetal.,2001;Lambert,2011).

Primatesarethusessentialagentsofforestdynamicsand regeneration, contributing to the maintenanceof high biodiversity of tropical ecosystems. As aconsequence, their extirpation could significantlyimpactonrecruitmentpatternsofmanyplantspecies(Lambert, 2011), which would lead to populationcollapse and in the long term to a shift in the plantcommunity(Terborghetal.,2008;Babweteeraetal.,2009; Poulsen, 2009). It has been argued that largegut-sized birds, such as hornbills, must have a highsubstitution capacity for primate seed dispersal, bydispersing the same set of seed species. However,hornbillstendtousehigherstrataofthecanopyforestandareattractedbyfruitsofdifferentcolors,feedingmoreoftenonreddishfruitspecies,whereasprimatesprefer brown and green fruits (Poulsen et al., 2002).Thus, dispersal redundancy between these two taxaisdebatablealthoughitseemsclearthatnoonetaxoncouldcompletelyreplacetheother(Poulsenetal.,2002;Lambert,2011).Moreover,redundancyamongspeciesbelongingtoclosely-relatedtaxaisnotalwayshigh.IntheDjaBiosphereReserve,apesandCercopithecines(Cercopithecus, Lophocebus and Colobus) exhibita small overlap in the seed species they disperse,leadingtotheconclusionthatthelossofseeddispersalservicesbyapescouldnotbecompletelyfulfilledbyCercopithecines(Poulsenetal.,2001).

To highlight the importance of primates for seeddispersal, Lambert (2011) used a powerful approachtodemonstratetheecologicalnecessityofconservingprimates for forest dynamics and biodiversitymaintenance. She applied themulti-species umbrellaconcept for ecosystem conservation. An umbrellaspecies is by definition “a species for which itsconservation confers protection to a large numberof naturally co-occurring species” (Roberge et al.,2004, page77). The originality of her study was towork at higher taxonomic ranks than the speciesand to implement in her definition the importantmutualism existing among plants and animals. Inthatway, the conservationof an umbrella taxonwillbenefitmanyspecies,bothfloralandfaunal.Basedonspecies richness within taxa, abundance, sensitivityto human disturbance and visitation rate of fruitingtrees,primatesprovedtobethemostfitting“umbrella


taxon” compared to birds and squirrels. In terms ofseed dispersal and its role in themaintenance of thehigh biodiversity of tropical forests, conservationefforts targeted towards primates therefore representanadequatemanagementshortcutinsituationswhereconservingallanimalandplantspeciesiseconomicallyimpossible. Currently, almost half of the world’sprimate species face conservationchallenges (IUCN,2012). The application of the above managementstrategy would be therefore highly relevant for thefutureofmanyprimatespecies,includingthecriticallyendangeredwesternlowlandgorilla.

3.2. Western lowland gorilla seed dispersal

Toourknowledge,thefirstdocumentationofwesternlowlandgorilla seeddispersal activitywaspublishedtwodecadesago(Tutinetal.,1991a).Sincethen,onlyahandfulofstudieshaveprovidedfurtherinformationonthistopic,andmostofthemwereconductedatthesame study site as the initial study inLopéNationalPark, Gabon. Nonetheless, improved knowledge ofgorilla ecology contributes to the appreciation of itspotential quantitative and qualitative effectiveness inseeddispersal,asdiscussedbelow.

Quantitative dispersal.Intermsofquantitativeseeddispersal,thewesternlowlandgorillaislikelytoplayanimportantroleforthefollowingreasons:– They are regular fruit-eaters, feeding on a diverse set of species. In periods of fruit abundance, fruit consumptionaccountsforupto70%offeedingtime (Doran-Sheehy et al., 2009). Feeding ecology studies conductedacross its range (Ndoki,Congo; Lopé,Gabon;Mondika,CongoandCentralAfrican Republic; Bai Hokou, C.A.R.) have identified 70 to115fruitspeciesinthegorilladietateachstudy site(Doranetal.,2002).Fruitremainswerefound inalmosteveryfecescollectedovera7-yearperiod inLopé(96%,N=4,301feces;Tutinetal.,1993). Onaverage,onefecalclumpwasfoundtocontain remainsofthreedifferentfruitspecies;– With an average body weight reaching 90 and 180kg for adult females and males respectively (Caldecottetal.,2009),thewesternlowlandgorilla hasthelargestbodysizeofallprimatesoftheCongo basin.Dailyfoodintakerequiredformetabolismis thereforehighandbyextensiontheyareresponsible fortheremovalofalargeproportionofthefruit/seed crop. In the Dja Biosphere Reserve, Cameroon, despitethelowdensityofwesternlowlandgorillas comparedtothesixsympatricprimatespecies(the moustachedmonkeyCercopithecus cephus cephus, the white-nosed guenon Cercopithecus nictitans nictitans,thecrownedguenonCercopithecus mona pogonias, the black-and-white colobus Colobus

guereza occidentalis, the grey-cheeked mangabey Lophocebus albigena albigena and the central chimpanzeePan troglodytes troglodytes), they are assumedtodispersealonealmostasmanyseedsas the rest of the primate community as a whole (Poulsenetal.,2001).Withanaverageof40.8intact seeds per fecal unit (SD, ±262.6), a density of 1.7weanedindividuals.km-2[95%IC,1.0–2.9]and 6.7defecations per day, western lowland gorillas could be dispersing 464.7seeds per day per km2

[range,273.4–792.7]compared to664.2[422.4– 955.9]fortheremainingprimatecommunity.

Qualitative dispersal.Fromaqualitativeperspective,western lowland gorillas may also be effective seeddispersersbecause:– They usually process fruits in the mouth and gut without causing damage to seeds; fruit remains in feces consist mainly of intact and still viable seeds (Tutin et al., 1993; Poulsen et al., 2001; Doranetal.,2002).Manyseedspecieshaveahigh concentrationofsecondarycompoundsandgorillas lackthespecializationofthedigestivetractrequired tometabolize them(Rogersetal.,1990), resulting in the passing of most seeds through the gut undigested (Williamsonetal.,1990).Additionally, thegutsizeof thegorilla is largeenoughtoallow them to swallow the seeds of most fruit species they feed on. The longest-running study investigatingwesternlowlandgorillaseeddispersal identified70seedspeciespresent in feces samples over a 6-year period, encompassing 76.9% of the fruitspeciesknowntofeatureinitsdietatthissite (N= 91;LopéNational Park,Gabon:Tutin et al., 1991a; Tutin et al., 1991b). While chimpanzees, thesecondlargestprimateofCongoBasinforests, systematically expulse seeds exceeding 4.2cm3, seeds up to 7cm3 can be found in gorilla feces (Tutinetal.,1994).Seedsthatpassthroughwestern lowlandgorilla’sdigestivetractintactconservetheir germinationcapacity.Poulsenetal.(2001)observed apositiveeffectongerminationsuccessofUapaca seeds from passage through the western lowland gorilla gut. Germination success reached 62% after passage through the gut compared to a 26% germination success for seeds manually extracted fromfruitpulp.Amongthesixprimatespeciestested (fiveCercopithecinesand thecentralchimpanzee), the western lowland gorilla conferred the highest germinationenhancementforUapacaseeds;– Seedsareretainedforalongperiodinthewestern lowland gorilla digestive tract. In addition to the relationship between digestive tract length and body size, the type of food consumed along with theseedsinfluencesseedtransittime.Forinstance, anincreaseintheamountoffruitconsumedresults


in shorter retention time of the digesta (Traveset, 1998). The diet of the western lowland gorilla, thoughhighlyfrugivorous,includesnon-fruititems suchasleaves,pith,shoots,barksandinsectsyear round(Tutinetal.,1993)andininverseproportion to fruit consumption (Doran-Sheehy et al., 2009). Thismixed diet influenced by seasonality and the large body size of gorillas are responsible for relatively long though variable retention times of seeds in thedigestive tract regardlessofseedsize, rangingfromafewhours(<10h)to136h,witha mean of 47.1h (Remis, 2000). By comparison, central chimpanzees have a mean retention time of23.6h(Idani,1986)andtheoneofCercopithecine species ranges from 21.2h to 25.4h (Poulsen etal.,2001).Therelativelylongretentiontimeofthe western lowlandgorillamayenhancegermination, as demonstrated forUapaca seeds (Poulsen et al., 2001),ormayconverselyinhibitit(Traveset,1998). Finally, as a consequence of long and variable retentiontimescoupledwithlongdailypathlengths (from <1km to 5.3km; Remis, 1997), western lowland gorillas likely provide a complex heterogeneous seed shadow with an extended tail oflongdistancedispersal.Whilesuchanextended seedshadowincreasestheprobabilityofencountering suitable conditions for seedling recruitment, long distancedispersalalsofavorsmaintenanceofgenetic diversity and rate of range expansion of the plant populations concerned (Kollmann, 2000;Hardesty et al., 2006). The dispersal andmating system of individualgorillasfurthercontributestothis;when amaleleavesthenatalgroupinsearchoffounding a breeding group, this blackbackmalemay travel verylongdistances(Douadietal.,2007);– Seeds dispersed by the western lowland gorilla encounter particular environmental conditions. Westernlowlandgorillashaveabimodaldefecation patternwithhalfoftheirfecesproducedatnestsites andtheotherhalfduringdailydisplacement(Todd et al., 2008).Nest sites are not selected randomly and canopy openness seems to be a major determinant. Preference for open canopy areas for nesting,suchastreefallgaps,isaconstantfeature acrosstherangeofthewesternlowlandgorilla(e.g., Tutinet al.,1995;Mehlmanet al.,2002;Arnhem, 2008;Willie et al., 2012). Seeds dispersed at nest sites are thus likely to encounter microsites with higher light regimes than seeds dispersed during daily displacement. This seems to be particularly profitableforpost-dispersalseedfateaspointedout byTutinetal.(1991a)inLopé,Gabon.SeedsofCola lizaedispersedatnestsiteshadhighergermination success, seedling establishment and survival rate thanseedsdispersedelsewhere;71.6%ofseedlings survived at nest sites after two months compared

to 13.2% elsewhere. Although not systematically monitored, Cola lizae seeds deposited directly beneathparent trees, either throughoral expulsion byprimatesorfromfallenfruits,seemedtofacea muchhighermortalityratethandispersedseeds.The suitabilityofgorillanestsitesforpost-dispersalseed fatewasconfirmedfortwoadditionalspeciesatthe samestudysite(Ganophyllum giganteum[A.Chev.] Hauman [Sapindaceae] and Uapaca guineensis Müll.Arg. [Euphorbiaceae]: Voysey et al., 1999). Seedling survival and growth of these species werealwayshigheratnestsitesaftertwoyearsthan beneaththecrownofparenttreesorforthosescatter dispersedbyotherprimatespeciesatshortdistances fromtheparentalsource.Itseems,therefore,thatthe westernlowlandgorillamaybeauniquedisperserin terms of its “directed dispersal” (i.e. dispersal of seeds in microsites presenting environmental conditions particularly suitable for recruitment: Howe et al., 1982).Although directed-dispersal is thought to be a rare phenomenon, it leads to a muchhigherprobabilityofsurvivaltoadulthoodon aper-seedbasisthantheotherkindsofseeddispersal advantages (Wenny, 2001). In this particular situation, the animal species performing directed dispersalmay contribute significantlymore to the plantpopulationconcernedthanallotherdispersers. Themostexplicitexampleinthetropicscomesfrom malebellbirdsperchingpreferentiallyinopencanopy environment,which improves seedling survival of the tree, Ocotea endresiana Mez [Lauraceae] (Wenny, 2001). Regular dispersal of seeds by the westernlowlandgorillainopencanopysitesisalso likelytoimproverecruitmentsuccessoftreespecies asmostofthemrequireatleastsmallcanopygaps toreachadulthood.Interestingly,speciesrequiringa high light regime at seedling stage are most commonly found among timber species (Doucet, 2003).

The western lowland gorilla possesses biologicalandecologicaltraitsrequiredtoperformeffectiveseeddispersal. Transportation of many seeds away fromtheparentplant inopencanopyhabitatsmaygreatlyimproveseedandseedlingfateofmanytropicalspecies,and dispersal of large-seeded species contribute totheirspatialdistribution.Inregardsofthat,thewesternlowlandgorillaisagoodcandidateofbeingakeystoneelementoftheecosystem,likeelephantareconsideredtobe(Blakeetal.,2009).

It is worth noting, however, that the westernlowland gorilla may also influence its environmentby causing damages to recruits of woody species.Although terrestrial herbaceous vegetation composesthemajorityofgorillanests,inalmosteverystudysitesaplings, either bended or broken, are also common


nest building material (Tutin et al., 1995; Mehlmanetal.,2002;Willieetal.,2012).Thewesternlowlandgorillaisalsoresponsiblefordamagesbybreakingtheshoots for consumptionof the soft inner part, youngleavesandtheapicalbud.Forexample,Kouadio(2009)observed important seedling and sapling destructionin timber plantations. In order to debate on the realcontribution of one animal species on the ecosystemdynamicsitisimportanttoconsiderboththepositiveandnegativeeffectsthattheanimalspeciesexerts.Inthe present case, lack of empirical information andquantitativedataimpedebalancingbothcontributions.However,thelossoftheseeddispersalserviceofthewesternlowlandgorillaisbelievedtohavemuchmorenegativeimpactontheforestthandooccasionalrecruitdestructionasdiscussedinthenextsection.

4. WILDLIFE DEPLETION AND THE FUTURE OF TROPICAL FORESTS

Inthetropics,thehighoccurrenceofzoochoryleadstointerdependentdynamicsbetweenplantsandanimals,where disturbance affecting one taxon will havean impact on the other (Sodhi et al., 2009); habitatdisturbancemayresultinadecreaseinwildlifedensity(e.g. Poulsen, 2009), and depletion of wildlife mayalter regenerationpatternsofplantcommunities (e.g.Terborghetal.,2008).

Presently,forestsoftheCongobasinfaceincreasingratesofdegradation through increasedanthropogenicpressure on natural resources (forest conversion forfarming and agriculture, extractive industries, illegallogging, fuel-wood provisioning; deWasseige et al.,2012).Inadditiontothis,thebushmeatcrisisreachedapeakduetoanincreasinghumanpopulation,togetherwiththeimprovedroadnetworkandtheeasieraccessto fire-arms (Wright, 2010). In summary, forests aredeclininginsizeandwildlifeisdeclininginabundance.As frugivores representmost of the tropicalwildlifebiomass it is not surprising that they are the mostharvested taxon, encompassing82%of the carcassesfound on western and central African markets (Faet al., 2005). The same tendency is observed in theNeotropics,wherefrugivoresoftheAmazonianbasin,regardless of their size, decline faster in abundancewithincreasinglevelofhuntingpressurethantheotherdietaryspecializationgroups(Peresetal.,2007).Onlyrodents seem to increase in abundance with habitatdegradationandlargevertebrates’depletion(Malcolmetal.,2000;Poulsen,2009).

Degradationandhuntingcanleadtolocalextinctionsof frugivoreswith large-bodiedspecies facinghigherrisk(Pimmetal.,1988)as1) theynaturallyoccuratlowerdensitiesthansmallerspecies,2)theyoftenrelyon large continuoushabitat tracts, 3) theyhave slow

reproductiverates,4)theygivebirthtofeweroffspring,5)theyaremorevaluabletohuntersand6)theycannotadjusttopersistenthuntingpressurebybecomingmorebehaviorally inconspicuous (Babweteeraet al., 2007;Babweteeraetal.,2009;Poulsen,2009;Wilkieetal.,2011).Localextirpationoflarge-bodiedfrugivoreswillresultindispersallimitationoflarge-seededtreesgiventhat remaining smaller-bodied frugivoreswill not beabletoswallowanddispersethem(Wangetal.,2007;Blake et al., 2009; Vanthomme et al., 2010). Seedswill thensimplyfallbeneath thecrownof theparentplant and risk high density- or distance-dependentmortality(Janzen,1970;Connell,1971;Harmsetal.,2000;Seidleretal.,2006;Blakeetal.,2009;Poulsen,2009). Without transportation of seeds through thegut of a frugivore, the probability of encountering afavorablesiteforrecruitmentisreduced,thusresultingin recruitment limitation (Babweteera et al., 2007).Such altered patterns of tree recruitment could leadin the long-term to shifts in community structure(Seidleretal.,2006;Wright,2010;Wilkieetal.,2011),composition (Poulsen, 2009; Wright, 2010) and toreducedadulttreediversity(Blakeetal.,2009).

Recruitment limitation of large-seeded specieswill have another disruptive effect on the ecologicalfunction of tropical forests. Large seed size isgenerally associated with shade-tolerant long-livedspeciesbecauseseedlingswillrelyonseedresourcesfor establishment in a shaded environment, whilesmall seeds are associated with light-demanding,fast-growing and short-lived species (Queenboroughetal., 2009). Moreover, seed size is correlated towood density (Queenborough et al., 2009),which isa good predictor of carbon storage capacity (Ruiz-Jaen et al., 2011). Therefore, recruitment limitationof large-seeded long-lived tree speciesmay result ina plant community shift towards a higher density ofsmall-seededshort-livedtreespecies(Terborghetal.,2008;Vanthommeetal.,2010),resultingin turn inalowerrateofcarbonsequestration(Kirbyetal.,2007).

Like the other two charismatic largest frugivoresof Central Africa (elephants and chimpanzees), thewestern lowland gorilla is at risk of extinction,withhuntingpressureandhabitatloss/degradationbeingthemostwidespread threats (IUCN,2012); a riskwhichcouldrender theprecedingpossibilitiesareality.Notonly large-seeded tree species will be affected bythe loss of the service provided by these threatenedlarge frugivores but also zoochorous species, whichrecruitdisproportionately,betterinopencanopysiteswhere gorillas produce most of their feces. If thestrong declining trend of these keystone disperserscontinues, the effects on theCongo basin ecosystempresentedabovewillbeinevitable(Blakeetal.,2009).Obviously,survivaloftropicalforestsiscompromisedfirst and foremost by much more direct threats


imposing immediate effects on them.Satellite imagecomparisonsovertimereportanetannualdeforestationrate in Central Africa of 0.17% per year and anadditional0.09%ofdenseforestisdegradedannually(deWasseigeetal.,2012).Consideringalltheservicesprovided by forests to humans, such as provisioningof food, timber and non-timber forest products,and carbon sequestration, the loss and degradationof tropical forests is of great concern. In contrast tothe external threats, wildlife depletion impacts onthe forest from the inside.Although the degradationthroughdispersallimitationissubtlerwitheffectsthatrequireyearsbeforebeingmanifests,consequencesonecosystemgoodsandservicesarereal.Treecoveraloneisthereforenotasatisfyingmeasureoftheecosystemhealth. Instead, equilibriumof the dynamics existingbetweenplantsandanimalsshouldalsobetakenintoaccount(Terborghetal.,2008).

5. CONCLUSION

Theeffectivenessofprimatesasseeddispersalagentsiswidelyrecognizedand thewestern lowlandgorillashouldnotbeexcluded.Althoughpoorlydocumented,aninitialreviewofthephysiologyandecologyofthisAfrican great ape shows that this species fulfills themain requirements for effective seed dispersal, bothfrom the quantitative aswell as the qualitative pointofview.

A distinctive trait of thewestern lowland gorilla,which highlights its value as seed disperser, is itsspecificdispersal-relatedrelationshipwithatleastonetreespecies,Cola lizae,anextremelyrarephenomenon,whichmightbeprejudicialincaseofdisperserloss.Atpresent, it is unknown howmany such relationshipsmight exist between thewestern lowlandgorilla andotherplantspeciesintropicalforests.

Bydispersingseeds regularly in treefallgaps, thewestern lowland gorilla might be an active vectorof seed dispersal in light of the directed-dispersalhypotheses (Wenny, 2001). Empirical demonstrationof this particular advantage on the fitness of speciesdispersedbythewesternlowlandgorillawouldmakeitastrongcandidateforbeingakeystonespeciesforitsecosystem.

The limited yet revealing information availableonwesternlowlandgorillaseeddispersal,consideredalongsidetheinherentbiologicalandecologicaltraitsof thegorilla, clearly lead to the suggestion that thisape plays a substantial role in Afrotropical forestdynamics, population structure, and maintenance ofbiodiversity and ecosystem function.As the westernlowland gorilla is critically endangered and needsimmediateactiontobetakentopreventitsextinction,theemphasisonitsecologicalrolewithinitsecosystem

maybeusedinadditiontoitsflagshipstatusforfundraisingandpublicawareness.

Acknowledgements

The authors thank each institution that provided financialsupport to Charles-Albert Petre for his ongoing PhDresearch: theBelgianSciencePolicyOffice,AntwerpZoo(“Dehousse” scholarship), and the Fondation GouverneurRenéClose.

Bibliography

AndresenE.&LeveyD.J.,2004.Effectsofdungandseedsizeonsecondarydispersal,seedpredation,andseedlingestablishment of rain forest trees. Oecologia, 139(1),45-54.

ArnhemE., 2008. Réponse éco-éthologique des grandssinges et autres mammifères à l’exploitation forestière sélective au Cameroun. Thèse de doctorat:Université Libre de Bruxelles (Belgique), http://theses.ulb.ac.be/ETD-db/collect ion/available/ULBetd-11252010-100423/,(24/06/13).

AugspurgerC.K., 1984. Seedling survival of tropical treespecies: interactions of dispersal distance, light-gaps,andpathogens.Ecology,65(6),1705-1712.

BabweteeraF., SavillP. & BrownN., 2007. Balanites wilsoniana: regeneration with and without elephants.Biol. Conserv.,134(1),40-47.

BabweteeraF.&BrownN., 2009. Can remnant frugivorespecies effectively disperse tree seeds in secondarytropical rain forests?Biodivers. Conserv.,18(6),1611-1627.

BaskinC.C. & BaskinJ.M., 1998. Seeds: ecology, biogeography, and evolution of dormancy and germination.SanDiego,USA:AcademicPress

BlakeS.etal.,2009.Forestelephants: treeplantersof theCongo.Biotropica,41(4),459-468.

CaldecottJ. &MilesL., 2009. Atlas mondial des grands singes et de leur conservation.Paris:UNESCO.

ChapmanC.A., 1989. Primate seed dispersal: the fate ofdispersedseeds.Biotropica,21(2),148-154.

ChapmanC.A.&OnderdonkD.A., 1998. Forests withoutprimates:primate/plantcodependency.Am. J. Primatol.,45,127-141.

ConnellJ.H., 1971. On the role of natural enemies inpreventing competitive exclusion in some marineanimals and in rainforest trees. In: Den BoerP.J. &GradwellG.,eds.Dynamics of populations.Wageningen,TheNetherlands:PUDOC,298-312.

de WasseigeC. et al., 2012. Les forêts du bassin du Congo. État des Forêts 2010.Luxembourg:OfficedesPublicationsdel’Unioneuropéenne.

DoranD.M. et al., 2002. Western lowland gorilla dietand resource availability: new evidence, cross-site


comparisons, and reflections on indirect samplingmethods.Am. J. Primatol.,58(3),91-116.

Doran-SheehyD., MongoP., LodwickJ. & Conklin-BrittainN.L., 2009. Male and female western gorilladiet: preferred foods, use of fallback resources, andimplicationsforapeversusoldworldmonkeyforagingstrategies.Am. J. Phys. Anthropol.,140(4),727-738.

DouadiM.I. et al., 2007. Sex-biased dispersal in westernlowland gorillas (Gorilla gorilla gorilla). Mol. Ecol.,16(11),2247-2259.

DoucetJ.-L., 2003. L’alliance délicate de la gestion forestière et de la biodiversité dans les forêts du centre du Gabon.Thèsededoctorat:FacultéuniversitairedesSciencesagronomiquesdeGembloux(Belgique).

FaJ.E.,RyanS.F.&BellD.J.,2005.Huntingvulnerability,ecologicalcharacteristicsandharvestratesofbushmeatspecies in afrotropical forests.Biol. Conserv., 121(2),167-176.

GarberP.A. & LambertJ.E., 1998. Primates as seeddispersers:ecologicalprocessesanddirectionsforfutureresearch.Am. J. Primatol.,45,3-8.

GillespieR.G. et al., 2012. Long-distance dispersal: aframework for hypothesis testing. Trends Ecol. Evol.,27(1),47-56.

HardestyB.D., HubbellS.P. & BerminghamE., 2006.Geneticevidenceoffrequentlong-distancerecruitmentin a vertebrate-dispersed tree. Ecol. Lett., 9(5), 516-525.

HarmsK.E. et al., 2000. Pervasive density-dependentrecruitment enhances seedling diversity in a tropicalforest.Nature,404,493-495.

HoweH.F.&SmallwoodJ.,1982.Ecologyofseeddispersal.Annu. Rev. Ecol. Syst.,13,201-228.

IdaniG.,1986.Seeddispersalbypygmychimpanzees(Pan paniscus): a preliminary report.Primates, 27(4), 441-447.

IUCN,2012. IUCN red list of threatened species. Version 2012.2.,http://www.iucnredlist.org,(3/02/2012).

JanzenD.H., 1970. Herbivores and the number of treespeciesintropicalforest.Am. Nat.,104,501-528.

KirbyK.R.&PotvinC.,2007.Variationincarbonstorageamongtreespecies:implicationsforthemanagementofa small-scale carbon sinkproject.For. Ecol. Manage.,246(2-3),208-221.

KollmannJ., 2000. Dispersal of fleshy-fruited species: amatterofspatialscale?Perspect. Plant Ecol.Evol. Syst.,3(1),29-51.

Kouadio, 2009. Mesures sylvicoles en vue d’améliorer la gestion des populations d’essences forestières commerciales de l’Est du Cameroun.Thèsededoctorat:Faculté universitaire des Sciences agronomiques deGembloux(Belgique).

LambertJ.E., 2011. Primate seed dispersers as umbrellaspecies:acasestudyfromKibaleNationalPark,Uganda,with implications forAfrotropical forest conservation.Am. J. Primatol.,73(1),9-24.

LambertJ.E. & GarberP.A., 1998. Evolutionary andecologicalimplicationsofprimateseeddispersal.Am. J. Primatol.,45,9-28.

LetouzeyR., 1985.Notice de la carte phytogéographique du Cameroun au 1:500000 (1985). Toulouse, France:InstitutdelaCarteInternationaledelaVégétation.

LiebermanM. & LiebermanD., 1986. An experimentalstudyofseedingestionandgerminationinaplant-animalassemblageinGhana.J. Trop. Ecol.,2(2),113-126.

MalcolmJ.R. & RayJ.C., 2000. Influence of timberextraction routes on central African small-mammalcommunities, forest structure, and tree diversity.Conserv. Biol.,14(6),1623-1638.

MehlmanP.T. & DoranD.M., 2002. Influencing westerngorillanestconstructionatmondikaresearchcenter.Int. J. Primatol.,23(6),1257-1285.

Müller-LandauH.C. et al., 2008. Interspecific variationin primary seeddispersal in a tropical forest.J.Ecol.,96(4),653-667.

NathanR. et al., 2008.Mechanismsof long-distance seeddispersal.Trends Ecol. Evol.,23(11),638-647.

NchanjiA.C.&PlumptreA.J.,2003.Seedgerminationandearlyseedlingestablishmentofsomeelephant-dispersedspecies in Banyang-Mbo Wildlife Sanctuary, south-westernCameroon.J. Trop.Ecol.,19(3),229-237.

PeresC.A.&PalaciosE.,2007.Basin-wideeffectsofgameharvestonvertebratepopulationdensitiesinAmazonianforests:implicationsforanimal-mediatedseeddispersal.Biotropica,39(3),304-315.

PimmS.L.,JonesH.L.&DiamondJ.,1988.Ontheriskofextinction.Am. Nat.,132(6),757-785.

PoulsenJ.R., 2009.Logging and hunting alter patterns of seed dispersal and seedling recruitment in an afrotropical forest.PhDdissertation:UniversityofFlorida(Florida,USA).

PoulsenJ.R.,ClarkC.J.&SmithT.B.,2001.Seeddispersalby a diurnal primate community in the Dja Reserve,Cameroon.J. Trop. Ecol.,17,787-808.

PoulsenJ.R., ClarkC.J., ConnorE.F.& SmithT.B., 2002.Differential resource use by primates and hornbills:implications for seed dispersal. Ecology, 83(1), 228-240.

QueenboroughS.A. et al., 2009. Seed mass, abundanceandbreeding systemamong tropical forest species:dodioeciousspeciesexhibitcompensatoryreproductionorabundances?J. Ecol.,97(3),555-566.

RemisM.J., 1997. Ranging and grouping patterns of awestern lowland gorilla group at Bai Hokou, CentralAfricanRepublic.Am. J. Primatol.,43,111-133.

RemisM.J., 2000. Initial studies on the contributions ofbody size and gastrointestinal passage rates to dietaryflexibilityamonggorillas.Am. J. Phys. Anthropol.,112,171-180.

RobergeJ.-M. & AngelstamP., 2004. Usefulness of theumbrellaspeciesconceptasaconservationtool.Conserv. Biol.,18(1),76-85.


RobertsonA.W., TrassA., LadleyJ.J. & KellyD., 2006.Assessingthebenefitsoffrugivoryforseedgermination:the importanceof thedeinhibitioneffect.Funct. Ecol.,20(1),58-66.

RogersM.E.etal.,1990.GorilladietintheLopéReserve,Gabon:anutritionalanalysis.Oecologia,84,326-339.

Ruiz-JaenM.C.&PotvinC.,2011.Canwepredictcarbonstocks in tropical ecosystems from tree diversity?Comparing species and functional diversity in aplantation and a natural forest. New Phytol., 189(4),978-987.

SeidlerT.G.&PlotkinJ.B.,2006.Seeddispersalandspatialpatternintropicaltrees.PLoS Biol.,4(11),e344.

ShepherdV.E. & ChapmanC.A., 1998. Dung beetles assecondaryseeddispersers:impactonseedpredationandgermination.J. Trop. Ecol.,14,199-215.

SodhiN.S.,BrookB.W.&BradshawC.J.A.,2009.Causesand consequences of species extinctions. In: LevinS.,ed.The Princeton guide to ecology.Princeton,NJ,USA:PrincetonUniversityPress,514-520.

TerborghJ.etal.,2008.Treerecruitmentinanemptyforest.Ecology,89(6),1757-1768.

ToddA.F., KuehlH.S., CipollettaC. &WalshP.D., 2008.Usingdung toestimategorilladensity:modelingdungproductionrate.Int. J. Primatol.,29(2),549-563.

TravesetA.,1998.Effectofseedpassagethroughvertebratefrugivores’ guts on germination: a review. Perspect. Plant Ecol. Evol. Syst.,1(2),151-190.

TravesetA., RobertsonA.W. & Rodriguez-PerezJ.,2007.A review on the role of endozoochory in seedgermination.In:DennisA.J.,SchuppE.W.,GreenR.A.& WescottD.A., eds. Seed dispersal: theory and its application in a changing world.Wallingford,UK:CABInternational,78-103.

TutinC.E.G., WilliamsonE.A., RogersM.E. &FernandezM., 1991a.A case study of a plant-animalrelationship:Cola lizaeandlowlandgorillasintheLopeReserve,Gabon.J. Trop. Ecol.,7,181-199.

TutinC.E.G. et al., 1991b. Foraging profiles of sympatriclowlandgorillasandchimpanzeesintheLopéReserve,Gabon.Philos. Trans. R. Soc. Lond., Ser. B,334,179-186.

TutinC.E.G. & FernandezM., 1993. Composition ofthe diet of chimpanzees and comparisonswith that ofsympatriclowlandgorillasintheLopeReserve,Gabon.Am. J. Primatol.,30,195-211.

TutinC.E.G.& FernandezM., 1994. Comparison of foodprocessing by sympatric apes in the Lope Reserve,Gabon. In: ThierryB., AndersonJ.R., RoederJ.J. &HerrenschmidtN., eds. Current primatology. Vol. 1: ecology and evolution. Strasbourg, France:UniversitéLouisPasteur,29-36.

TutinC.E.G., ParnellR.J., WhiteL.J.T. & FernandezM.,1995. Nest building by lowland gorillas in the LopeReserve, Gabon: environmental influences andimplicationsforcensusing.Int. J. Primatol.,16(1),53-76.

ValentaK.&FediganL.M., 2009.Effects of gut passage,feces, and seed handling on latency and rate ofgermination in seeds consumed by capuchins (Cebus capucinus).Am. J. Phys. Anthropol.,138(4),486-492.

VanthommeH., BelléB.& ForgetP.-M., 2010. Bushmeathuntingaltersrecruitmentoflarge-seededplantspeciesinCentralAfrica.Biotropica,42(6),672-679.

VoyseyB.C. et al., 1999. Gorillas and seed dispersal inthe Lope Reserve, Gabon. II: survival and growth ofseedlings.J. Trop. Ecol.,15(1),39-60.

WangB.C., SorkV.L., LeongM.T. & SmithT.B., 2007.Huntingofmammalsreducesseedremovalanddispersalof the Afrotropical tree Antrocaryon klaineanum(Anacardiaceae).Biotropica,39(3),340-347.

WennyD.G., 2001. Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol. Ecol. Res., 3,51-74.

WilkieD.S.,BennettE.L.,PeresC.A.&CunninghamA.A.,2011.Theemptyforest revisited.Ann. N.Y. Acad. Sci.,1223(1),120-128.

WilliamsonE.A., TutinC.E.G., RogersM.E. &FernandezM.,1990.CompositionofthedietoflowlandgorillasatLopeinGabon.Am. J. Primatol.,21,265-277.

WillieJ.,PetreC.-A.,TaggN.&LensL.,2012.Densityofherbaceousplantsanddistributionofwesterngorillasindifferent habitat types in south-east Cameroon.Afr. J. Ecol.,51(1),111-121.

WillsonM.F., 1993. Dispersal mode, seed shadows, andcolonizationpatterns.Vegetatio,107/108,261-280.

WrightS.J.,2010.Thefutureoftropicalforests.Ann. N.Y. Acad. Sci.,1195(1),1-27.

(71ref.)

Documents

Role of the western lowland gorilla (Gorilla gorilla ... et al_author...Role of the western lowland gorilla (Gorilla gorilla ... ... 3, 3