Implications of body mass and predation for ape social system andbiogeographical distribution

Julia Lehmann and Robin Dunbar

J. Lehmann (j.lehmann@roehampton.ac.uk) and R. Dunbar, Brit. Acad. Centenary Res. Project, School of Biological Sciences, Univ. ofLiverpool, Liverpool, L69 7ZB, UK. JL also at: School of Human and Life Sciences, Roehampton Univ., Whitelands College, London, SW154JD, UK. RD also at: Inst. of Cognitive and Evolutionary Anthropology, Univ. of Oxford, Oxford, OX2 6PE, UK.

Despite the fact that all African great apes have overlapping diets, they differ substantially in both biogeographicaldistribution and social organisation: Gorilla lives in relatively small, cohesive groups within a small biogeographical areawhile Pan is much more widely distributed and lives in large, fluid groups in which the members are rarely all together. Inthis study we use a modelling approach to identify possible causes and consequences of these differences. We use a timebudget model which is based on the relationship between time available for various activities, group size, body mass andclimate. We demonstrate the importance of body mass as a critical determinant for maximum ecologically tolerable groupsize as well as ape distribution patterns. In addition, we show that predation pressure may play a strong role in limitingthe distribution of smaller-bodied apes (Pan). Predation pressure appears to be especially important if the apes opt for afission�fusion strategy because it obliges them to maintain larger (sub-) groups. In effect, the apes appear to face a tradeoffbetween solving the predation problem by increasing body size (at the expense of reduced ecological flexibility) and goingfor ecological flexibility (but at some cost in terms of how they handle predation).

One of the main goals in the study of animal social systemsis to understand the interaction between a species’ specificecological needs, its social organization and its biogeogra-phical distribution patterns. It is generally thought that thesocial organisation of a species reflects both ecologicalpressures, such as predation pressure and the distribution offood and mates, and a species’ phylogenetic history (Brooksand McLennan 1991, Harvey and Pagel 1991) while thebiogeographical distribution reflects ecological constraints.However, in some cases we find that although species havestrong phylogenetic relationships and similar ecologicalrequirements, they can differ significantly in their socialorganisation and/or biogeographical distribution. Oneexample of this is African apes: despite their closephylogenetic relationship (Di Fiore and Rendall 1994),their largely overlapping diets (Tutin and Fernandez 1993,Stanford and Nkurunungi 2003, Morgan and Sanz 2006)and their occurrence in similar habitats (Kingdon 1971),they differ in their distribution range and have verydissimilar social organisations. Gorilla lives in small,cohesive groups that centre round an alpha male (Schaller1963, Jones and Sabater Pi 1971), while Pan lives in muchlarger fission�fusion societies which are characterised bytheir fluid nature, i.e. the individuals of these large groupsare rarely seen together at one place but usually spendtheir time in much smaller subgroups (so-called parties)(Reynolds and Reynolds 1965, Nishida 1968, Sugiyama1968, Wrangham 1979, Goodall 1986). In addition, the

biogeographical distribution of Gorilla is much morelimited than that of Pan (Caldecott and Miles 2005),although the exact reasons for this are unknown.

Thus, in the present study, we ask to what extentecological constraints (such as predation risk) and morpho-logical constraints (such as body mass) affect ape biogeo-graphy and social organisation. These two factors are notusually considered in this context but may be cruciallyimportant. While body mass may affect the maximumnumber of individuals that can live within one social group(due to intragroup competition), predation pressure mayplace a constraint on the minimum group size needed in agiven habitat to successfully overcome risk of predation(Hill and Dunbar 1998). In cases where required minimaexceed possible maxima some habitats may indeed becomeuninhabitable for a species (Dunbar 1996) even though itappears to be suitable based on other ecological parameters.Such constraints might be especially important for taxa likePan that, due to their fission�fusion social system, spendmost of their time in small sub-groups, which may bevulnerable to predation.

In the present study, we use an existing and validatedtime budget model for African great apes (Lehmann et al.2008a) to determine how these two previously ignoredvariables, i.e. body size and predation risk, interact to setlimits on apes’ ecological range and social organisation. Wespecifically ask whether these constraints can explain whyGorilla has a much smaller geographical range than Pan.

Oikos 118: 379�390, 2009

doi: 10.1111/j.1600-0706.2008.16382.x,

# 2009 The Authors. Journal compilation # 2009 Oikos

Subject Editor: Tim Benton. Accepted 4 September 2008

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The time budget model (Lehmann et al. 2008a) allows us toassess the relative importance of the extent to which theabove factors are responsible for the differences in theirbiogeography and social organisation. The model assumesthat animals are limited by the amount of time they need tofulfil their daily physiological requirements, namely feeding,resting, travelling and socialising (the latter being importantfor group cohesion). The time needed to do so depends onthe ecological conditions (i.e. climate), competitive regime(i.e. group size) and morphological parameters. Thus, thismodel is ideally suited to identify ecological and morpho-logical constraints on ape maximum ecologically tolerablegroup size and hence biogeography, which in turn may alsoexplain differences in social organisation (Ghiglieri 1987).Using a similar model, Lehmann et al. (2007a) have shownthat behavioural strategies, such as fission�fusion (wheregroups regularly split into much smaller subgroups) can beused to overcome ecological limits on group size: in Pan,fission�fusion sociality enables individuals to increase groupsize beyond their ecological limits (Lehmann et al. 2007a).However, these differences in social organisation betweenPan (fission�fusion) and Gorilla (usually in a cohesive socialgroup) do not explain observed biogeographical distribu-tion patterns of the two taxa.

In this study we use the model to ask (1) how does bodymass affect ape distribution patterns, (2) how does bodymass affect group size and social organisation and (3) canpredation pressure explain ape biogeographical distributionpatterns?

Material and methods

Background information about the ape model

Full details of the great ape model used in this study, aswell as its derivation and validation, are given in Lehmannet al. (2008a). The model is intended to determine themaximum ecologically tolerable size of a group that, undergiven ecological conditions, a population can maintain as acoherent social unit. This output variable can then in turnbe used to determine biogeographical distribution patterns.

Time budget models like this have been used previouslywith great success to model primate biogeography (Dunbar1992a, 1992b, Williamson and Dunbar 1999, Hill andDunbar 2002, Korstjens and Dunbar 2007, Lehmann et al.2007a, 2008a, 2008b). These models work on the assump-tion that, because the amount of daytime is fixed, an animalhas to balance its nutritional intake and expenditure whiletrading off the different time budget components (namelyfeeding, moving, resting and grooming time). To modeldifferences in social organisation realistically our ape model(Lehmann et al. 2008a) distinguishes between the group(i.e. the relatively stable set of individuals who share acommon range area) and the party (i.e. the often unstableset of individuals who feed, rest or travel together at anygiven moment). In Gorilla, groups and parties are usuallyone and the same, while in Pan, parties are usually a subsetof the group and thus significantly smaller in numerical size(Goodall 1968, Nishida 1979, Boesch and Boesch-Acher-mann 2000). While maximum ecologically tolerable groupsize is the output variable of our model, average party size,which has been shown to be driven by (amongst otherfactors) ecological conditions such as food distribution(Wrangham 1977, 2000, Wrangham et al. 1992, Chapmanet al. 1995, Boesch 1996, Matsumoto-Oda et al. 1998), isdetermined by climatic conditions and forest cover (Leh-mann et al. 2008a). Because this model is not species-specific, it uses species body mass and group biomass asindependent variables. Unless otherwise stated, Pan wasmodelled using an average biomass of 40 kg, while we useda value of 120 kg for Gorilla. The model also includes dietcomposition, which can differ between the ape species(usually there is less fruit available to Gorilla as compared toPan). Diet is estimated from an equation based on bodyweight and ecological conditions fitted to data for actualpopulations (Table 1).

In the model, we assume that feeding and moving timeare independently determined by climate, diet, body mass,party/group size, while grooming time is determined by asimplified version of a generic grooming equation definingthe amount of time that is needed to maintain the socialcoherence of a group of a particular size through time(Lehmann et al. 2007b). Similarly, we calculated enforced

Table 1. Statistical values for equations used in the model.

Variable Equation1

% fruit in diet (%fruit) 169.43�50.65�log(bm)�0.021�alt�62.02�moimomx�0.39�forestcover

% leaves in diet (%leaf) 100�%fruitGroup biomass (grpbm) 4.24�bm�29.83�group sizeAverage party size (B80 kg) 21.49�0.072�forestcover�0.33�Pmo�0.0012�(Pmo)2

Average party size (�80 kg)* Group sizeMin party size chimp2 e(2.25�0.23�ln(forest

cover)�0.36�ln(T

ann))/3

Min party size gorilla2 e(2.25�0.23�ln(forestcover

)�0.36�ln(Tann

))/7% feeding 33.09�0.005�grpbm�0.14�bm�0.16�%fruit�0.006�Pann

% moving 18.74�13.92�TmoSD�0.35�prtysz�4.94�(P2T)�0.32�(P2T)2

% resting �29.47�1.28�Tann�0.34�%leaf�5.95�TmoSD% grooming 1.01�0.23�group size

1 equations from Lehmann et al. (in press a) (see text for details)+ because most gorillas travel as one group rather than splitting up into smaller parties party and group size are considered to be the same;minimum group/party sizes are scaled to female body weight bm�body mass; alt�altitude; moimomx �maximum monthly moisture index(Willmott and Feddema 1992); prtysz�average party size; forestcover�percentage forest cover (derived from DeFries et al. 2000); Pann�mean annual rainfall in mm; Tann�mean annual mean temperature in 8C; TmoSD�temperature variation between months (calculated as thestandard deviation across average values for 12 months); Pmo�average rainfall per month in mm; P2T�plant productivity index (the numberof months in the year in which rainfall [in mm] was more than twice the average monthly temperature, Le Houerou 1984).

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resting time (which is a consequence of the fact that animalsneed time to digest food and are unable to engage inenergetically costly activities when ambient temperaturesrise above a critical threshold) by using a generic equationderived from a comparative study using 78 species ofprimates (Korstjens et al. unpubl.).

Figure 1 shows a flow diagram for the ape model usedin this study, the core equations for which are given inTable 1. All equations used in the model are derived fromobservational data collected on wild great ape populations(Lehmann et al. 2008a).

Procedure

The model uses the equations in Table 1 to calculate, foreach of the sites in our location database, the maximumecologically tolerable group size. The model starts with agroup size of one individual and calculates that individual’stime budget by using the equations in Table 1. If the sum ofthe time budget variables does not exceed 100%, group sizeis then increased algorithmically by one individual at a timeuntil the sum of all time budget variables exceeds 100%; themaximum ecologically tolerable group size is then definedas the group size of the previous cycle (see Dunbar 1992bfor details on the procedure).

Apes are considered to be able to live at a particular site ifthe predicted maximum ecologically tolerable group sizeexceeds a set minimum viable group size: for Pan,minimally required group size was set to 10 individuals(because almost all known Pan populations live in groupslarger than this, reviewed by Lehmann et al. 2007a), whilethis limit was set to five individuals for Gorilla (five is theminimum group size for known Gorilla group, reviewed byLehmann et al. 2008b).

All analyses (unless other wise stated) are based on ‘realworld’ climate data as the ape model was run using a largeclimate database for Africa (obtained from Willmott andMatsuura 2001) which provides a continuous climatedataset on a grid of 0.58 latitude and 0.58 longitude acrossAfrica. This dataset consists of 10 075 data points andallows us to ‘experimentally’ test the effects of body massand predation risk on ape group sizes and distribution

patterns (below). A second dataset consisting of 639 sub-Saharan locations for which climate conditions as well asthe presence and absence of apes is known was used tocompare model predictions with actually observed data ongroup sizes. Unless otherwise stated, the model allowed Pan(i.e. small bodied apes) to split into smaller parties (fission�fusion) while Gorilla was modelled as a more cohesivegroup to model the observed differences in ape socialorganisation.

Effects of body mass on ape biogeographyTo evaluate the importance of body mass for apebiogeography and group sizes, we ran the model on thelarge climate dataset, predicting ape group sizes anddistribution patterns as a function of body mass across thewhole of sub-Saharan Africa. We used body masses of 30,40, 50 and 80, 120 and 160, which roughly correspond tothe variation in body weights of female, average and maleweights for Pan and Gorilla respectively (Caldecott andMiles 2005). Because the two taxa in the original model alsodiffer in terms of their social system (fission�fusion vscohesive groups), direct comparisons of the resulting groupsizes in Pan and Gorilla are difficult, as we have previouslyshown that fission�fusion enables Pan to increase theirecologically tolerable group size (but has very little influenceon biogeographical distribution per se; Lehmann et al.2007a). Thus, to be able to directly compare predictedgroup sizes across the different body mass conditions, wealso ran the model with a restriction preventing all apesfrom employing a fission�fusion social system (in whichcase average party size equalled group size for all weightconditions), allowing us to compare directly across therange of body masses.

Effects of body mass and social organisation on ape groupsizesTo evaluate the effects of fission�fusion social organisationon ape time budgets and hence overall group size, we usedthe equations in Table 1 and calculated time budgets forPan and Gorilla with and without fission�fusion, therebydetermining empirically the effects of subgroup formation

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Precipitation

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Bodyweight

Diet(%fruit)

Biogeography

Predation

Figure 1. Flow chart of the relationships between climate, ape diet, body weight, group size and time budget variables as used in themodel. Solid arrows indicate relationships used in the model, dashed arrows indicate relationships that are ‘optional’, depending on thestrategy used by a species and dashed-dotted arrows indicate interdependency in climate variables which, however, were not used in thismodel. True independent variables are those in grey boxes.

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on time budgets and the possible maximum group size. Forthis particular analysis, climatic conditions were heldconstant (realistic average values derived from Pan studysites were used) because we are primarily interested in theeffects of fission�fusion on time budgets and group size, noton the effects of climatic conditions per se. By keepingclimate constant, we can compare the effects of fission�fusion on virtual sympatric apes of different body sizeswithin the same environment.

Effects of predation risk on ape biogeographyPredation pressure has been identified as one of the maindrivers for primate sociality (van Schaik 1983, Dunbar1988, Hill and Dunbar 1998, Shultz et al. 2004, Dunbarand Shultz 2007). Although apes do not suffer high rates ofpredation, a significant risk of predation does still exist(Boesch 1991, Tsukahara 1993, Fay et al. 1995). In light ofthis, it has been argued that a certain minimum group size isrequired to ensure sufficient protection against predators(Dunbar 1996, Hill and Dunbar 1998). In fission�fusionspecies, this would set a lower limit to the smallest size ofparty that would be viable in a given habitat. To determinewhether predation risk has an effect on ape biogeography,we introduced a new constraint to our model: average partysize predicted by the model must be larger than theminimum party size required to ensure sufficient protectionagainst predation. Because there is very little directinformation on ape predation risk which would haveallowed us to estimate minimum group size based onclimatic conditions, we calculated minimum party sizeusing an equation from Dunbar (1996) which estimatesminimum group size in baboons based on forest cover (acorrelate of refuge availability) and bush cover (a correlateof the risk of being caught unaware by a predator). Sincepredation risk is also a function of body mass (large animalsare susceptible to a smaller range of predators: Dunbar1988), we scaled the values for minimum group sizepredicted by this equation by the ratio of ape body size tobaboon body size (baboons were considered to be 1/3 of thesize of Pan and 1/7 of the size of Gorilla). Forest cover wasobtained from a satellite database (DeFries et al. 2000)while bush cover was calculated using the equation based onclimatic variables given by Dunbar (1996) (Table 1). Inorder to determine whether minimum party size was aboveor below average predicted party size, we calculated the ratioof average feeding group size (�party for Pan) to minimumrequired group size, so that a value �1 indicates thataverage party size is larger than the minimum requiredgroup size and a value B1 indicates that average party sizeis smaller than minimum group size. We assumed that apesare only able to survive in habitats where the ratio is equalto or larger than 1.

Effect of predation pressure on ape biogeographyBecause predation pressure is inherently difficult to quantify,we approximated it by collating information on the presenceand absence of apes and their major predators (lions andleopards) for a dataset of 185 African locations. Lions andleopards have both been reported to attack apes (Boesch1991, Tsukahara 1993, Fay et al. 1995). The data on lion andleopard presence/absence were obtained from either

the primary literature or UNEP databases (UNEP-WCPA/<http://www.unep-wcmc.org/wdpa//>). Frequency of ob-served co-residence of apes and their predators werecompared to predicted patterns. Finally, to assess whetherpredator distribution patterns affect ape distribution, wevisually analysed overlaps in distribution patterns usingpublished distribution maps for lions, leopards and apes.

Statistics

We used a linear program in Dbase to run the ape model,calculating maximum ecologically tolerable group size foreach location in our dataset. Mann�Whitney U-tests(MWU) and student’s t-tests (TT) were used to comparevariables between correctly and incorrectly predicted sites,while ANOVA in combination with the LSD posthoc testwas used to analyse the effects of body mass on diet andgroup size. Log-likelihood goodness-of-fit statistics and x2-tests were used to compare correct and incorrect modelpredictions and frequencies of co-residence of predators andPan, respectively. All analyses were done using SPSS 14.0for Windows.

Results

Effects of body mass on ape biogeography

Figure 2 shows the predicted biogeographical distributionof apes as a function of body mass, with body mass chosento represent male and female Pan (Fig. 2a) and Gorilla (Fig.2b): this suggests that the heavier the ape, the morerestricted its distribution. Note that biogeographical trendscorrectly reflect the variations in weight between differentchimpanzee and gorilla subspecies: western chimpanzees arethe smallest (Morbeck and Zihlmann 1989, Groves 2001),followed by eastern chimpanzees (Morbeck and Zihlmann1989, Groves 2001), while the central chimpanzees are thelargest (Groves 2001). This corresponds directly to thedistribution patterns indicated in Fig. 2: when overall bodymass is increased, apes are no longer predicted to occur atwestern sites, followed by the loss of eastern sites when bodymass is increased further. Similarly, mountain gorillas whoare the heaviest of all gorillas only range in eastern Africa,which according to the model is the one habitat capable ofsustaining the heaviest animals. This suggests that theweight differences between ape subspecies are crucial fortheir distribution patterns. Body mass also has a strongimpact on maximum ecologically tolerable group size itself.

Figure 3 depicts median group sizes predicted by themodel for locations within the apes’ actual distribution, forvarious body masses. Group sizes differ significantly acrossbody mass conditions (ANOVA F�914.9, DF�3/6072,pB0.0001; all post hoc comparisons: pB0.001). As can beseen in Fig. 3, even under the non-fission�fusion condition,group sizes decline with increasing body weight, indicatingthat large bodied apes are only able to maintain relativelysmall cohesive groups. However, note that the animals’ability to exploit a fission�fusion strategy allows them toincrease group size and exaggerate the effect of body masson group size.

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Effects of body mass and social organisation on apegroup sizes

Figure 4 shows how, irrespective of body weight, apes couldincrease maximum ecologically tolerable group sizes bysplitting into smaller subgroups (foraging parties): both taxacould thus increase their group sizes significantly by fission�fusion. However, smaller-bodied apes will benefit more byemploying a fission�fusion strategy as they will gain moreindividuals than larger apes would, and they do so despitethe fact that larger-bodied apes gain an advantage through

reduced feeding time requirements by being able to exploita more leaf-based diet as a result of doing so (equations inTable 1). Body size thus seems to be an important factorinfluencing both group size and the absolute benefitsderived by fission�fusion sociality.

Effects of predation risk on ape biogeography

The results presented here focus on Pan, as this is the onlytaxon for which the inclusion of minimum party sizes had a

Figure 2. Effects of body weight on virtual ape distribution patterns: (a) light grey area�Pan female (30 kg) and both dark grey areas�Pan male (50 kg); darkest shading indicates groups larger than 45 individuals; (b) light grey area�gorilla female (80 kg) and dark greyarea�gorilla male (160 kg); panel (a) and (b) also depict the present day distribution of Pan and Gorilla (black outline); dashed linesindicate major rivers (possible geographical barriers for the distribution of large bodied apes).

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significant effect. The more cohesive Gorilla group sizeswere usually above the critical minimum level.

Figure 5 depicts Pan biogeographical distributionpatterns predicted by the model, incorporating the effectsof minimum party size, with ‘high risk sites’ (sites at whichthe ratio of average party size to estimated minimum partysize is below 1) in light grey. Overall, minimum predictedparty size is significantly higher at sites for which Panpresence was incorrectly predicted (i.e. outside the taxon’scurrent distribution) as compared to correctly predictedpresence sites (i.e. those within Pan’s biogeographicaldistribution) (MWU: n�2612, z��20.6 pB0.0001;minimum party size within Pan distribution: four indivi-duals; minimum party size at false positive sites: fiveindividuals). At those locations where minimum party sizeexceeds average party size, predation risk might forcepopulations to travel in parties that are actually largerthan the optimal size for balancing time budgets. This inturn may restrict overall group sizes because individualsmight have to compromise on social cohesion (by spendingless time on social interaction than they ought to).

Note that the distribution of Pan is now limited in thesouth by a wide belt of high risk habitat running eastwardsas far as the Rift Valley in central Africa. This may explainwhy the bonobo’s (Pan paniscus) distribution is restricted inthe south to the Congo basin even though there seems to beviable habitats for them further south in northern Angolaand Zambia. Figure 5 also suggests that the chimpanzeepopulations currently inhabiting many West African loca-tions may be under considerable stress from predationpressure (an effect that may be enhanced by low levels offorest cover).

In our model, both predation risk and average party sizeestimates are linked to forest cover. In the former case,forest cover provides protection from predators while in thelatter case forest cover is likely to reflect food distribution.To assess the interactive relationship between forest coverand minimum and average party size estimates, we plottedestimated minimum party size (as predicted by the modelfor the smaller dataset of 639 sub-Saharan sites) and averageparty sizes (predicted for the same sites under the conditionof constant rainfall using a pmo-value of 100 ml) againstforest cover (Fig. 6). The two regression lines cross at 38%forest cover, which represents the limit below which Panmay not be able to survive because in such habitatsminimum required party size exceeds average party size. Ifwe compare the percentage of forest cover at sites where Panis known to occur with that from sites where Pan is absent,we find that forest cover is significantly lower at the lattersites than at the former (Fig. 7: TT: t��14.8, n�118,354, DF�470, pB0.0001).

In addition, the box plot in Fig. 7 shows that very fewPan sites have forest cover values lower than 38%; in fact,the inter-quartile range of the Pan distribution has a lowerbound of 37% for forest cover, supporting the model’spredictions that Pan will not be able to survive at sites withless than 38% forest cover. Moreover, sites for which themodel wrongly predicted Pan to be present have signifi-cantly lower forest covers than sites where Pan is known tooccur (TT: t�10, n1�141, n2�354, DF�493, pB0.0001; Fig. 7). Thus, predation risk (and linked withthis also forest cover) appears to be an important factorlimiting ape biogeographical distribution patterns.

Effect of predation pressure on ape biogeography

We categorised sites according to the presence or absence ofleopards and lions, both of which have been reported toattack and kill chimpanzees. Table 2 shows that, althoughthere is no difference in the distribution patterns of leopardsand Pan (x2�1.56, DF�1, n�185 p�0.6), Pan andlion distributions show little overlap (x2�3.51, DF�1,n�185, pB0.07). More importantly, Pan very rarelyoccurs at sites which have more than one of these predatorspecies (Table 2; x2 for chimpanzees present�24.4, DF�2, n�42, pB0.0001). Visually comparing publisheddistribution maps for lions, leopards and Pan shows thatthe presence of Pan is negatively correlated with thepresence of lions (but not that of leopards) � even for sitesat which, according to the model, Pan could live. Interest-ingly, most of the areas for which the model wronglypredicts Pan to be present are sites where both leopards and

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Figure 4. Effects of body mass and fission�fusion on maximumecologically tolerable group sizes in Pan and Gorilla.

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Figure 3. These boxplots show the effects of body weight ongroup size. Only locations within the distribution of apes wereincluded. This illustrates how an increase in body mass reducesape group sizes (median) via effects on their time budgets. Forcomparative reasons the first dark grey bar shows predicted groupsize for a 40 kg ape with fission�fusion while all subsequent barswere derived from a model without fission�fusion (as this socialorganisation allows apes to increase overall group sizes beyondtheir ecological limits). FF�fission�fusion, nFF�no fission�fusion.

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lions occur (Fig. 8). This adds weight to the suggestion thatalthough Pan could (based on their time budgets) survive inthese areas, they may not actually be able to live therebecause they would need to maintain larger parties thanthey could realistically sustain in these habitats. Heavierapes, such as gorillas, show the same patterns as describedhere for Pan.

Discussion

Compared to previous time budget models (Dunbar 1992a,1992b, Williamson and Dunbar 1999, Korstjens et al. 2006,Korstjens and Dunbar 2007, Lehmann et al. 2007a,Lehmann et al. 2008b), this model adds new layers ofcomplexity by stressing the role of body mass and predationin the evolution of ape social systems and biogeography. Thefact that this model is a generic model for African apes, basedon body mass (rather than being species-specific) allows us toinvestigate the specific role of ecological (i.e. climate andpredation pressure) and morphological (body mass) variablesin primate evolutionary history. We demonstrate that bodymass is a crucial predictor for the maximum ecologicallytolerable group sizes that ultimately limit ape biogeographi-cal ranges and social systems. Although fission�fusion socialorganisation allows apes to live in groups larger thanotherwise possible, predation pressure counteracts this byobliging apes to maintain larger parties, thereby substantiallylimiting their biogeographical range.

Effects of body mass on ape biogeography

Since our model does not distinguish a priori betweenspecies or genus, it is remarkable that both group size

predictions and biogeographical distribution patterns arecorrectly reflected for the two ape taxa considered here. Thisemphasises the overall importance of body mass for apesociality and biogeography, as this is the only independentinput variable other than climate in the model. In addition,the effects of body mass on group size and biogeography areexacerbated by a number of direct and indirect knock-onconsequences of body mass, such as increases in feedingtime, a dietary shift towards a more leaf-based compositionin heavier animals (which in turn affects resting time) andeffects of body mass on metabolic rates (Peters 1983). It hasalso been suggested previously that increased body massallows the storage of more fat and hence enables a species tosurvive in highly unpredictable habitats (Wheatley 1982).However, our finding of body mass restricting biogeogra-phy is not in line with this suggestion.

Even though not all of these knock-on effects of bodymass are included in the model, the model correctly reflectsspecies-specific differences in biogeographical distributionpatterns, suggesting that most of these differences can beexplained by body mass variation. Indeed, the model evenreflects the more subtle differences in subspecies body mass:West African chimpanzees, the lightest of the chimpanzee(excluding bonobo) subspecies (about 10�20 kg lighter thancentral African chimpanzees, Caldecott and Miles 2005) areamong the first to disappear from the map when body massis increased in the model. Similarly, under the highest bodymass condition the model correctly predicts apes to bepresent in reasonably large groups only in the range ofeastern gorillas (the heaviest of the gorillas) and south of theCongo River (which gorillas cannot get to because of theriver), indicating that time budgeting problems restrictthese large apes to the regions around the Virungamountains.

Figure 5. Effects of minimum party size on Pan distribution in tropical Africa: light grey � locations at which minimum party size �average party size; dark grey � locations at which minimum party sizeBaverage party size; black polygons indicate present day Pandistribution while dashed lines indicate major rivers.

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According to our model, the Congo basin (the areawithin the loop of the Congo River) is prime ape habitat: itis the habitat for which the largest groups are predicted.Interestingly, the apes found in these areas, bonobos, arerelatively small but live in large and fairly cohesive groups(White and Burgman 1990, White 1992, Chapman et al.1994, Stanford 1998, Hohmann et al. 1999), suggestingthat, in terms of evolutionary history, this might be analternative strategy (as compared to increasing weight) forcontrolling predation risk. On the other hand, the westernparts of central Africa can only support apes up to about100 kg body mass in reasonably large groups, and indeedwestern lowland gorillas are reported to be much lighterthan mountain gorillas (Caldecott and Miles 2005). These

results suggest that the observed east�west differences in apebody mass might be of more important than has beenpreviously realised as they may significantly restrict thebiogeographical distribution of subspecies.

Both ape taxa show a large degree of sexual dimorphismwith males weighing up to twice as much as females (Smithand Cheverud 2002). Our model suggests that thedistribution of males (i.e. the heavier sex) is much morelimited than the distribution of the lighter females, so thatfemales, in theory, could range over a wider area than males.The overall distribution of apes might thus be restricted bythe ability of the heavier males to fulfil their time budgetrequirements. This constraint could work in two (non-exclusive) ways � either females stay with males forprotection (‘hired guns’: Rubenstein 1986) and hence limittheir own range to that of the heavier males, or alternatively,females make use of a larger range, but this in turn limitsthe number of males that can live within the group. Thelatter hypothesis is based on the ecologically plausibleassumption that the limiting factor is indeed party biomassand not individual body weight. If this is the case, then weshould expect competition between species to exacerbatethis effect. Although there is some evidence to suggest thatfeeding competition does occur between gorillas andchimpanzees at some sites (Tutin et al. 1991, Stanfordand Nkurunungi 2003), there are insufficient data toinclude this effect in the model. However, if gorillas’ accessto ripe fruits is affected by the presence of chimpanzees (andother primates), it may well affect both their time budgets(note that resting time will increase when the percentage ofleaves in the diet increases: Lehmann et al. 2008b) andgroup sizes, and hence further restrict their distribution.

Group size, body mass and ape social system

Our model demonstrates that group size in apes is criticallydependent on body mass. It is not clear why Gorilla hasopted for such a large body mass, but their large size forcesthem to live in relatively small social groups. However,without the capacity to exploit a fission�fusion system, evensmaller-bodied Pan could only maintain groups of about 30individuals (Fig. 4). Thus, rather than being an emergentproperty of Pan societies due to ecological selectionpressures, it appears that fission�fusion sociality may be ameans whereby Pan can push group size beyond theecologically imposed limits (Lehmann et al. 2007a).Although this is in line with previous arguments that socialstructure is not necessarily a direct consequence of ecology(Wrangham 1986), it remains puzzling why Gorilla doesnot also use fission�fusion as a strategy to increase groupsize. One possible reason might be that gorillas, due to theirlarge body mass, would not actually benefit from main-taining a higher order group structure. Although the actualbenefits gained by Pan from doing so remain unclear, it ishighly likely that the nature of these benefits dependscritically on species body mass and diet so that large-bodiedapes do not benefit to the same extent from increasinggroup size. If, for example, group size is important for Panto defend a feeding territory of a size that ensures that theyalways have sufficient fruits available, then gorillas may notneed such large groups since they do not rely on fruits and,

806040200

8.00

6.00

4.00

2.00

0.00

Forest cover (%)

Part

y si

ze (

indi

vidu

als)

Figure 6. This graph shows how party size (black circles) andminimum party size (black crosses) correlate with forest cover.Party size was calculated for a constant Pmo-value of 100 ml tominimises the confounding effects of climate. The graph showsthat minimum party size exceeds average party sizes in habitatswith less than 38% forest cover.

False presencePresentAbsent

80

60

40

20

0

For

est

cove

r

Figure 7. Forest cover of sites where Pan are absent, present andpredicted to be present but absent in reality. This graphdemonstrates that very few Pan populations live in habitats withless than 38% forest cover. It also shows that the majority of falsepositive predictions are for sites with less than 38% forest cover.

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hence, do not need to defend a feeding territory. Inaddition, the overall gain in group members by usingfission�fusion as a strategy is considerably smaller in larger-bodied apes (Fig. 2) and may not generate sufficient gain inbenefit.

Predation pressure, which is bound to act on the level ofthe party (i.e. the set of individuals that actually foragestogether) and not at the overall group level, is almostcertainly not the reason for increasing overall group (i.ecommunity) sizes beyond their ecological limit in the waythat a fission�fusion strategy allows in Pan. Rather, theopposite seems to be the case: our model indicates thatpredation pressure may play a strong role in limiting thedistribution of apes if these opt for a fission�fusion strategy:predation pressure may then oblige them to maintain largerparties than ecologically possible, thereby limiting theirdistribution. In the case of gorillas, it may well be thatfissioning into smaller groups would provide a disadvan-

tage, so that fission�fusion as a strategy to increase overallgroup size may be too costly. It has been suggested thatcohesive gorilla groups are a consequence of females seekingmale protection against harassment (Wrangham 1979) andinfanticide (a form of predation pressure) (Harcourt andGreenberg 2001). If that is the case, this may provide astrong selection pressure preventing cohesive gorilla groupsfrom splitting into smaller subgroups.

Finally, some gorilla populations have been reported tooccasionally split into subgroups, while peaceful feedingaggregations have been reported from Bai habitats (Tutin1996, Doran-Sheehy et al. 2004). Furthermore, Bradleyet al. (2004) reported that individual gorilla groups mayactually be part of a larger dispersed gorilla kin network,suggesting that a higher order social structure may exist inthis taxon. With this in mind, one could argue that gorillastoo live in some kind of fission�fusion social system, butone which, in comparison to Pan, is much less flexible

Table 2. Co-occurrence of predators and Pan at a set of sub-Saharan sites. Numbers are percentage of Pan /non-Pan sites at which predatorsare present or absent. Numbers in parentheses are frequencies.

Leopards Lions No. of predators

Pan Present Absent Present Absent 1 Present 2 Present Absent

Present 79 (33) 21 (9) 29 (12) 71 (30) 69 (29) 19 (8) 12 (5)Absent 76 (108) 24 (34) 44 (63) 56 (79) 38 (54) 41 (59) 21 (30)

Figure 8. Comparison of predicted biogeographical distribution of apes with distribution patterns of their main predators (lions andleopards).

387

because subgroup size is strongly constrained by femalesocial strategies, diet and/or predation pressure. Thissuggestion is supported by the finding of Lehmann et al.(in press b) that gorilla feeding time is more stronglyaffected by population density than by group size.

In sum, then, the apes appear to face a tradeoff betweensolving the predation/harassment problem by increasingbody size (at the expense of reduced ecological flexibility)and group cohesion, and going for ecological flexibility (butat some cost in terms of how they handle predation).

Predation and ape biogeography

As outlined above, predation appears to have a significantinfluence on ape biogeography as it is always a serious riskin primates. Although predation events in apes are relativelyrare, this does not necessarily imply that the risk (asopposed to rate) of predation does not play a significantrole in the evolution of their social systems (Hill andDunbar 1998). Indeed, it has been suggested that predationpressure explains differences in grouping patterns betweeneast and west African chimpanzees: while chimpanzees inGombe, Mahale and Budongo (East Africa), which do nothave any natural predators, are often found alone or insmall family parties (Wrangham and Smuts 1980, Newton-Fisher et al. 2000, Itoh and Nishida 2007), chimpanzees inthe Taı forest (west Africa), where leopards are abundantand prey on chimpanzees, form larger and more cohesiveparties (Boesch and Boesch-Achermann 2000, Lehmannand Boesch 2004).

Because fission�fusion species are especially vulnerable tothe potential effects of predation (as they spend most oftheir time in very small subgroups), we included theminimum group size required to provide sufficient protec-tion from predators (Dunbar 1996) in our model. Since thisgave a marked improvement in biogeographical fit, itsuggests that predation is an important factor limiting greatape distributions. Incidentally, we found that, for mostareas immediately adjacent to present day distributionlimits, predicted minimum group sizes were larger thanpredicted sub-group size, suggesting again that predationpressure may indeed limit Pan distribution patterns. Thisappears to be especially important for the southerndistribution limits, where our original model overestimatedthe distribution of Pan (Fig. 3). Although suitable habitatfor apes, these areas are separated from the actual southernlimit of Pan by a belt of relatively open habitat for whichpredicted minimum group size is larger than predictedaverage party size (Fig. 5). Predation pressure may thus beone of the reasons why the range of Pan does not extendfurther south than it does. This is further supported by thefinding that Pan distribution patterns are negativelycorrelated with the presence of lions and that Pan are rarelyfound in habitats where lions and leopards co-occur. Notethat this is not just a by-product of the fact that Pan lives inforests: some Pan populations live in much more opensavannah-like habitats (Uehara et al. 1992, Pruetz et al.2002). Finally, the fact that both, minimum and averageparty size depend on forest cover suggests that the relation-ship between forest cover and party size is in fact U-shaped,

with larger parties needed in open areas (due to predationrisk) and larger parties possible in areas with dense forest(where food is more abundant) (Dunbar 1988). The troughof this U-shaped function (i.e. the point where the tworegression lines in Fig. 6 intersect) is identical to the lowerlimit of the inter-quartile range of forest cover at sites wherePan is known to exist. This supports our view that openhabitats, even though they may have suitable riverineforests, are not always viable habitats for Pan because theywould have to trade off their fission�fusion lifestyle (andthereby their larger groups) against more cohesive (andhence smaller) groups because of predation pressure. As thiswould ultimately result in smaller groups, such a strategymight not be feasible for Pan because they thereby lose thebenefit provided by large groups. Our finding that theminimum viable Pan group size appears to be around 45individuals, and that this can only be achieved with afission�fusion social system (Lehmann et al. 2007a),reinforces this suggestion.

These effects are in principal independent of body size,however, because even though gorillas do not usually splitinto smaller parties, their group sizes are in general largerthan the minimum group size required; hence, in contrastto Pan, predation pressure does not appear to limit theirdistribution.

Conclusions

Our study is one of very few studies to investigate whichfactors naturally limit the biogeographical distribution ofAfrican apes. Our model demonstrates that in addition togeographical barriers, body mass, and predation risk arecritical variables limiting the ecological range of Africanapes. One solution to counter the body mass dependentdecrease in maximum ecologically tolerable group sizes is toadopt a fission�fusion social system; however, the benefitsof such a system may critically depend on diet (Dunbar1988, Lehmann et al. 2007a). Predation pressure, on theother hand, appears to limit the extent to which groups canfission and hence seems to have played a major role inshaping ape sociality, despite the suggestion that their largebody size reduces overall predation risk.

Acknowledgements � JL was funded by the British AcademyCentenary Research Project, and RD is supported by a BritishAcademy Research Professorship. We also thank Amanda Korst-jens for general discussion about modelling procedures.

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