ORIGINAL ARTICLE

Food competition in captive female sooty mangabeys(Cercocebus torquatus atys)

Received: 5 March 2002 / Accepted: 18 October 2002 / Published online: 15 April 2003� Japan Monkey Centre and Springer-Verlag 2003

Abstract We studied the social and foraging behavior oftwo captive groups of sooty mangabeys under two dif-ferent spatial food situations. These food conditionswere clumped (food was placed in a box) and dispersed(food was dispersed over the entire enclosure). In eachgroup five adult females and two adult males wereobserved. As a criterion for food competition, individualdifferences in the relative food intake were used. Adultfemale mangabeys had a linear, stable, and unidirec-tional dominance hierarchy. Access to food was rankdependent among females only under clumped fooddistribution, as current models of the evolution of pri-mate social systems predict. However, feeding successappeared to be mediated not by female but by maleagonistic behavior toward females. High-rankingfemales received relatively less aggression from malesand could, therefore, stay and feed longer in the feedingarea. Male tolerance of higher-ranking females seems tomediate female feeding success under restricted foodresources. The establishment of a special relationshipwith a high-ranking male might, therefore, be a strategyto get better access to food. This study demonstratesthat female competition for access to food should not beanalyzed separately from male influences on females andsuggests that a more integral role of males in socioeco-logical models of the evolution of primate social systemsshould be considered.

Keywords Food competition Æ Dominance Æ Socialtolerance Æ Mangabeys

Introduction

Competition is generally regarded as one of the maincomponents of natural selection (Keller and Lloyd1992). In most animals, the sexes compete for differentkey resources that limit their reproductive success(Trivers 1972). Therefore, Wrangham (1979) suggestedfor group-living primates linking ecological factorsprimarily to female–female rather than to male–maleor male–female relationships. Wrangham (1980) intro-duced a socioecological model on the evolution of socialsystems in primates that assumes a causal relationshipbetween diet and its distribution in space and time,dominance system, and migration pattern. This modelwas extended by van Schaik (1989). In this model, pre-dation pressure is regarded as the ultimate factor ofgroup life per se and food competition among femalesespecially within groups as the main ultimate force of theinner structure of the group (van Schaik 1989; van Hooffand van Schaik 1992).

Van Schaik (1989) distinguishes between two types ofcompetition: scramble and contest. He defines foodcompetition as of the scramble type if individuals cannoteffectively exclude others from a common resource. Theresource tends to be shared equally (e.g. leaves formountain gorilla, Gorilla gorilla beringei: Watts 1988),and food intake success and therefore reproductivesuccess negatively depend primarily on group size. VanSchaik argues that aggression over food and coalitionsand alliances between females are not effective inimproving access to food. Hence, during the course ofevolution, females should develop individualistic andegalitarian dominance hierarchies, and agonistic supportshould be rare and not kin dependent. [cf. non-female-bonded (NFB) social system: Wrangham 1980].

Contest-type food competition occurs if the distri-bution of food resources [especially fruit trees; e.g. long-tailed macaques (Macaca fascicularis): van Schaik andvan Noordwijk 1988] allows some animals to excludeothers from obtaining a greater share of the resource

Primates (2003) 44:203–216DOI 10.1007/s10329-002-0012-x

Daniel Stahl Æ Werner Kaumanns

D. Stahl (&) Æ W. KaumannsDeutsches Primatenzentrum Gottingen, Germany

D. StahlYerkes Regional Primate Research Center, Atlanta, GA, USA

Present address: D. StahlDepartment of Primatology,Max Planck Institute for Evolutionary Anthropology,Deutscher Platz 6, 04103 Leipzig, GermanyE-mail: stahl@eva.mpg.de

than otherwise. Aggressive behavior gives rise to differ-ences in access to food. Highly differentiated socialstructures of the female-bonded (FB) type (cf. Wrang-ham 1980) should evolve: females should form coalitionswith kin to increase their power to monopolize a foodresource, resulting in a linear, stable, unidirectional, andmatrilineal dominance hierarchy within the group.Female reproductive success should be positively influ-enced by female rank within the group.

Van Schaik’s socioecological model withstood eval-uation by field studies in many cases (Sterck et al. 1997;for a review of alternative models: Matsumura 2001).However, most primate field studies are of a descriptivenature and can therefore only provide evidence for theinfluence of ecological factors on social structures.Intraspecific phenotypic variation of food competitionand other patterns of social behavior do not simplydepend on the ecological factor ‘‘food distribution’’ butalso on demographic factors and confounding variables,for example, predation pressure (van Schaik 1989; Bar-ton et al. 1996). Thus methodological difficulties arise inthe study of the causal link between food distributionand social system in group-living primates, and con-trolled experimental studies are needed as an importantextension to descriptive field studies (van Hooff and vanSchaik 1992). A quantitative experimental study on foodcompetition under strictly controlled conditions isalmost impossible in the wild. For this reason we chosean experimental study on food competition with captiveprimates to test hypotheses derived from the van Schaikmodel. If food competition is a deciding factor in theevolution of social systems, then the resulting basiccompetitive structures should be found in captive studiesas well. A recent field study by Range and Noe (2002)showed remarkable similarities of dominance structuresand of female social relationships of wild sooty man-gabeys compared to the social system described bycaptive studies.

The van Schaik model will be used to predict howindividuals of a group of primates behave in their dailylife under different environmental conditions. Thecomparison between expected and observed behaviorallows a discussion about the general acceptance of thesocioecological model for the evolution of social struc-ture.

Van Schaik’s socioecological model as well as arecent extension by Sterck et al. (1997) did not considerthe influence of males on females’ feeding success. Al-though van Hooff and van Schaik (1992) discussed thepossibility that males might supply females with food bydefending territories or food patches, almost all studiesfocusing on female food competition in primates onlyanalyzed female–female relationships. Furthermore,adult males are always present in groups and competefor food as well (cf. Clutton-Brock 1977). Males mightaffect females’ feeding success (e.g. Janson 1988) andshould be considered as a confounding variable. Forthese reasons, we analyzed the adult males’ behavior aswell.

As research subjects for a study on female socialrelationships we chose sooty mangabeys because oftheir rather unusual social system. Sooty mangabeyslive in West Africa, ranging from Liberia to Senegal(Schwartz 1921; Struhsaker 1971). They live in multi-male–multi-female groups with males considerablylarger than females. Group size ranges from approxi-mately 15 (Sierra Leone: Harding 1984) up to 90animals (Ivory Coast: Bergemuller 1998). Their large(approximately 8 km2) home ranges overlap consider-ably (Bergemuller 1998). Sooty mangabeys are frugi-vourous, and agonistic interactions over food itemswere observed in the field (Bergemuller 1998; Rangeand Noe 2002).

Mangabeys are in general described as FB species(van Hooff 1988). Research on captive sooty mangabeyshas shown that there is indeed a stable, linear, unidi-rectional hierarchy among females as expected for a FBspecies (Gust and Gordon 1994; Stahl 1998; Stahl andKaumanns 1999). A stable, linear hierarchy with unidi-rectional dominance relationships among adult femalesooty mangabeys was also observed in a field study byRange and Noe (2002).

Yet, captive sooty mangabeys do not exhibit amatrilineally based social structure as shown in FBspecies: affiliative (Ehardt 1988), aiding (Gust andGordon 1993), reconciliation (Gust and Gordon 1993),and tolerant (Stahl 1996) behavior as well as dominancerank (Gust and Gordon 1994) among adult females arenot kin dependent.

Furthermore, aiding among females is low comparedto female rhesus monkeys, a ‘‘classic’’ FB species (Gustand Gordon 1993). Sooty mangabeys, therefore, showbehavioral features that are typical for an NFB speciesas well. Since the social system of sooty mangabeyscannot be classified clearly as either FB or NFB, itsstudy can provide a promising tool to assess the pre-dictive power of van Schaik’s model.

In this experimental study, food intake and socialbehavior of two groups of sooty mangabeys wereinvestigated under two different conditions. The firstfeeding condition allowed each individual access to foodsimultaneously and was expected to induce mainlyscramble-type competition. The second feeding condi-tion allowed only a few animals to feed at the same timeat the food resource and was expected to induce contest-type competition.

It is hypothesized that if sooty mangabeys areadapted to contest food competition sensu van Schaik(1989), females should compete for access to foodunder clumped food distribution. A female’s socialposition should affect access to food under clumpedbut not under dispersed food distribution. The differ-ential feeding success among females should be medi-ated by direct competition between females. Changesin the variance of feeding success should be positivelyassociated with rates of aggressive and submissivebehavior (Janson and van Schaik 1988; van Schaik1989). If sooty mangabeys are adapted to an envi-

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ronment in which mainly scramble food competitionhas played an important role in shaping the species’social structure, then the range of behavior expressedin this study should fall within some species-specificphylogenetic constraints. Therefore, if mangabeys areadapted to scramble competition, there should be noeffect of social position on access to food. In a speciesadapted to scramble competition we expect that ago-nistic interactions should not be associated with thetype of food distribution, as it was shown in captivestudies with NFB primate species (Presbytis obscurus:Kerscher 1991; Papio hamadryas: Gore 1993; Zinner1993).

Methods

Study groups

Two social groups of sooty mangabeys (Cercocebus torquatus atys)were observed in the outdoor enclosures at the Field Station of theYerkes Regional Primate Research Center in Lawrenceville nearAtlanta, Georgia, USA. All mangabeys were descendants of agroup of 27 animals (Bernstein 1971).

The groups were living in compounds of the same size and withsimilar arrangements. The outdoor enclosures in which all obser-vations took place had a surface area of 225 m2 (15x15 m). Nor-mally the animals had access to water ad libitum, commercialmonkey chow twice (morning and afternoon), and fruit once(afternoon) daily.

The group size of 21 and 23 animals, respectively, and theirmulti-male–multi-female group composition resembled small tomedium-sized natural mangabey groups. At the onset of thestudy, group S1 consisted of two adult males, five adult females,four subadult males, two juvenile males, four juvenile females,and three infants. One infant was born during the study. GroupS3 was made up of two adult males, six adult females, twosubadult males, one subadult to adult female, two juvenile tosubadult females, three juvenile males, two juvenile females, andone infant (see Table 1 for details). Four infants were bornduring the study. The assignment to age classes was based onGust (1994).

Experimental design

During the experimental period, the animals were observed duringtwo different feeding conditions, clumped and dispersed. Bothgroups were accustomed to feeding under clumped and dispersedfood distributions during a preliminary experimental test phase,which lasted 3 weeks. Regular feeding by the caretakers alsoincluded rather clumped (pellets were distributed outside the fencefor a length of about 3–4 m) and dispersed (fruits were evenlydistributed over most of the compound) feeding conditions.

Under both feeding regimes the animals were observed daily,twice during feeding (morning and afternoon feeding sessions) andonce outside feeding times. Non-feeding sessions took place 15 minafter the end of the morning feeding observations. It was duringthis time period that animals were the most active outside offeeding sessions.

Feeding conditions

Under ‘‘clumped’’ food distribution, food was placed in a box(62·18·10 cm, length xwidth x height) fixed outside the fence.Only afew animals (up to four to five adult animals) could eat at the sametime directly at the food box. Under ‘‘dispersed’’ food distribution,foodwas evenly distributed inmost parts of the outdoor enclosure. Acaretaker distributed the pellets from an observation tower while thefirst author started recording the behavioral data. A pilot studyshowed that under dispersed distribution animalswere distributed allover the compound, moving around and feeding in a more or lessundisturbed way (Stahl 1998). A monopolization of food by one ormore animals was not observable.

Only standard primate pellets were fed during the food com-petition experiments. The use of pellets allowed an accurateassessment of the amount an animal ate.

Food competition was accomplished by restricting food to theamount they actually needed and could eat within an hour or less.The amount of food was determined during a test phase. Thisamount of food was enough to ensure that all animals did getenough food but forced the animals to feed and compete within the1-h observation period. All food was eaten within this time period.

The well-being of the animals was of first priority. Everyweekday an independent observer, who knew the groups well,visually checked all animals’ state of health. Furthermore, allanimals of a group were weighed once before and during aclumped food distribution session to ensure that no animal lostweight.

Table 1 Focal animals ofgroups S1 and S3: shown aresex, age in years at onset of thestudy, rank in its sex class,average weight (in kilograms)used for estimating basalmetabolism rate (BMR),estimated daily BMR(kilojoules per day), and meancorrection value for females dueto reproductive state for eachof the four observations blocks(Cl clumped. Di dispersed fooddistribution; 1 and 2 first andsecond observation periodunder type of distribution)

Animal(code)

Sex Age inyears

Rank Averageweight (kg)

BMR(kJ/day)

Correction value for BMR

Cl 1 Di 1 Cl 2 Di 2

Group S1Sgo M 8 M1 13 1,965Rgo M 8 M2 13 1,965Wco F 14 F1 7.55 1,307 1.25 1.5 1.5 1.5Veo F 10 F2 8.5 1,429 1.15 1.15 1.15 1.15Ilo F 4 F3 6.5 1,168 1.5 1.5 1.5 1.5Blo F 4 F4 6.8 1,209 1.44 1.5 1.5 1.5Fdo F 13 F5 7.3 1,275 1 1 1 1

Group S3Pfo M 10 M1 13 1,965Jgo M 9 M2 11.9 1,833Mdo F 15 F1 9.0 1,491 1.25 1.42 1.5 1.5Cho F 9 F2 9.1 1,498 1.25 1.34 1.5 1.5Ugo F 9 F3 9.6 1,559 1.15 1 1 1Zko F 5 F4 7.7 1,327 1 1 1 1Zgo F 9 F5 8.4 1,410 1.4 1.4 1.4 1.5

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Observation procedures

Focal animal sampling (Altmann 1974)

Focal animal sampling was used to collect behavioral data. Ineach group seven animals (two adult males and five adultfemales, see Table 1) were in focus. One adult female of groupS3 was blind and therefore not included as a focal animal.During a focal observation an animal was observed for 10 min.Its behavior was recorded continuously. Observations concen-trated on an individual’s foraging and food intake behavior andits agonistic relations and grooming behavior with all othergroup members. Under clumped food distribution it wasrecorded how long the animals stayed within the ‘‘feeding area’’(area within a radius of 2 m around the food box) and withintouching distance (<0.5 m) of the ‘‘food box’’. In addition, theduration the focal animal stayed together with other focal ani-mals at the food box was determined.

The different types of aggressive and submissive behavioralinteractions were categorized into aggressive and submissivebehavior. Submissive behavior included avoidance behavior. Thefollowing behaviors were recorded:

– Behaviors associated with ‘‘aggression’’: threat stare, headbob, lunge, displace, charge, chase, slap (hit), grab, pin toground, tail bite, other bites, fight

– Behaviors associated with ‘‘submission’’: avoid, move away,submissive present, tongue flickering, fear grimace, redirectthreat, crouch, flee

Most definitions were taken from unpublished manuscripts byD. Gust and I. Bernstein; a detailed description of the behavioraldefinitions is published in Stahl (1998). For each focal animal themean active aggressive and submissive behavior toward (a) focaladult males and (b) focal adult females during a 10-min focalobservation was calculated. Interactions with other non-adultanimals of the group were recorded and analyzed but are notpresented here (Stahl 1998).

Observation schedules

During each of the three daily observations blocks (morningfeeding, non-feeding, and afternoon feeding sessions) six 10-minfocal animal samplings were done. The order of the focal animalswas changed randomly during each observation block. Undereach feeding condition the animals were observed twice about6 weeks in a row. Within a 60-min feeding session every focalanimal was observed in a 10-min focal animal sampling at eachperiod of time (0–10th min, 11–20th min, ..., 51st–60th min) atleast three times and therefore in each 10-min-block under eachfeeding and non-feeding condition at least six times. Each animalwas observed for at least 6 hours during each morning feeding,non-feeding, and afternoon feeding session under each fooddistribution type. Animals of group S1 were observed 120 daysduring a 7-month period, and animals of group S3 were observed116 days during a 6-month period. Under both feeding conditionsanimals were observed twice in rotating order to distribute theeffect of season equally.

Instantaneous scan sampling (Altmann 1974)

During feeding times the entire group was rapidly scanned (about30 s) at the end of each 10-min focal animal observation bymarking the positions of the animals in a copied drawing of theenclosure. The positional behavior data were used to determineproximity patterns between males and females.

Following Zinner et al. (1997) we used the relative number ofcertain positional behaviors (e.g. staying in the feeding area with anadult male) after a 10-min observation block as a measure ofduration for the previous 10-min observation block.

Data analysis

Focal animal and instantaneous scan samples were not included inthe analyses if a female was in peak estrous, to minimize the effectsof estrous (Gust and Gordon 1991). During most of the time of thestudy the females were either pregnant or nursing their offspringand only few estrous (16 peak swellings from ten females) wereobserved. A separate analysis was, therefore, not possible.

Dominance relationships

Dominance relationships between focal animals were assessedfrom the distribution of dyadic aggressive and submissive inter-actions. Data of agonistic interactions were obtained from focalanimal sampling and additionally from ad libitum sampling. Adlibitum sampling was done opportunistically outside of the focalanimal sampling observations. As in the literature (Bernstein1976, Gust and Gordon 1994), a linear dominance hierarchy withmales dominant over females was easily established. Among theadult animals there were decided and temporarily stable domi-nance relations within each possible dyad independent of feedingcontext. Dominance relationships could be deduced by eitheraggressive or submissive interactions. No coalitions or alliancesagainst adult males were observed. For further details on domi-nance relationships see Stahl (1998) and Stahl and Kaumanns(1999).

Individual energy gain

Animals were fed entire pellets or parts of pellets. By counting thenumbers of fully eaten pellets and the number of bites of a pellet,the ingested energy gain could be estimated. Pellets weighted onaverage 1.85 g (dry weight) and contained 36 kJ of digestive energy(information from the producer, Harlan Teklad, Madison, Wis.,USA). In a preliminary test phase, bite size in relation to time wasestimated. Average bite size differed between the sexes and feedingconditions and decreased over feeding time. The decrease of bitesize over time was caused by animals having to feed more and moreon fragments of the original pellets. Therefore, energy gain had tobe calculated for each observation block for males and femalesduring the two feeding situations separately. Bite size was estimatedby counting the number of bites per fully eaten pellet. Fragmentsize was estimated by collecting and weighing pellet fragments atdifferent periods of times.

Energy gain was calculated for a 10-min block by the followingformula:

ingested energy ¼hX

ðwhole eaten pelletsÞ

þXðbites� bite sizeÞ

i� 36 kJ

Individual feeding success

Feeding success can be estimated by comparing the energetic gainwith the energetic need of an individual. Individual energetic needdiffers between animals and depends on several factors, such asbody weight, activity, reproductive status (for females), thermo-regulation, and growth. Therefore, to compare feeding successbetween individuals, a relative measurement of energetic need mustbe used.

For a comparison of feeding success the energy gain rate of ananimal was set in relation to its estimated basal metabolism rate(BMR). The BMR is the energy rate of a resting, not digestingbody within its temperature optimum, which is necessary tomaintain its function. In many species BMR is a linear functionof the logarithm of body weight (Kleiber 1961), which was con-firmed for non-folivorous prosimian primates (Muller 1985; Ross1992).

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Among females, BMR was adjusted for their reproductive state.Basal metabolism rate was increased during the latter stages ofpregnancy by 25% and during lactation by 50% (Lee and Bowman1995). If a female was only occasionally lactating we assumed anincrease of 15%. A pilot study following the methods of Coehloet al. (1976) showed that differences in energetic need due todifferent activity budgets were negligible in this captive environ-ment as was also seen in a captive study on hamadryas baboons(calculated from data of Zinner 1993).

Feeding success was measured by the amount of energy ananimal gained during a period of time in relation to its adjustedBMR:

relative energy gainðtÞ ¼ energy ingested ðkJ=tÞadjusted BMR ðkJ=24hÞ

where t is time period in hours, w is body weight of an animal inkilograms, c is the correction value for reproductive state offemales: 1.25 if pregnant, 1.5 if lactating, 1.15 if lactation is phasingout, and adjusted BMR=287·w0.75·c in kilojoules per 24 h.

The body weight is the mean of the weight measured before andnear the end of the study during the observations. Body weightcorrection value for reproductive state of females can be seen inTable 1.

Spatial male–female relationships

Male–female spatial relationships were analyzed during the first20 min of a feeding session under clumped food distribution. Todescribe spatial male–female relationships, instantaneous scansamples of positional behavior after the first and second 10-minfocal animal sampling were used to determine interindividual dis-tances between adult females and both adult males. The distanceswithin a dyad were classified into four distance categories (Ta-ble 2). Afterward, the relative number of scans in each categorywas calculated.

Because a single score is easier to use for analyses, a proximityindex for each female–male dyad was calculated. Following themethod of Perry (1997), the relative number of incidents of eachdistance category was multiplied with a weighting factor. Theweighting factor was derived by the reciprocal of the area eachdistance class covered. This method weights closer proximity moreheavily and takes into account the exponentially increasing chanceof being seen or being a target of a behavioral act with increasingproximity. Almost no agonistic behavior occurred between animalsat distances greater than 2 m during this observation period underclumped food distribution. Therefore these distances were regardedas a neutral distance and neglected. The method described by Perryfor wild arboreal capuchin monkeys was adjusted for the mainlytwo-dimensional structure of the enclosure and for the terrestrialbehavior of sooty mangabeys by using the reciprocal of the areaand not of a concentric sphere. The area of the first three categorieswas calculated by the following equation:

areacovered¼pr2u�pr2l

where ru is the radius of the upper limit of category n, and rl is theradius of the lower limit of category n.

For a better readability of the data the reciprocal of the areawas multiplied by p and then used as the relative weighting factor.

weighting factorcategory x ¼ 1=areacategory x � p

The proximity index P between two animals was then calculated by

P¼n1�4þn2�1:33þn3�0:33þn4�0

where n is the proportion of samples in the relevant category.

Statistics

Statistical analyses were carried out by using the program STAT-ISTICA for Windows 5.0, (StatSoft, Inc., 1996). Each focal animalwas observed under two experimental conditions to investigate theeffect of food distribution on its behavior. The same focal animalwas observed at a given focal observation period at least six times.We averaged these replicated observation scores to obtain a singlescore for each individual under each experimental condition forfurther analyses (Sokal and Rohlf 1995).

Two-factorial analyses of variances (ANOVAs) with a repeatedmeasure design were used for the analyses of focal females (n=10) todescribe the influence of two independent variables, food distribu-tion and group affiliation (Sokal and Rohlf 1995). Group affiliationwas included as an independent variable to reduce unexplained errorvariance. Correlations were done with Pearson product–momentcorrelation tests. For correlations involving members of bothgroups, the data were standardized by the mean of each group. Onlyrelative data were therefore used for these correlations.

Because of their higher power, parametric tests were preferredto non-parametric tests, although the relatively small sample sizemakes it difficult to evaluate the assumptions of such parametrictests. However, there were no outliers in the data set and data wereunimodally distributed and not seriously skewed. On that conditionthe used parametric tests are robust against deviations against theirtheoretical assumptions (Sokal and Rohlf 1995).

Statistical analyses including the males were done with non-parametric tests because of the small sample size (n=4). Analyseswith dependent variables were carried out with Wilcoxon matchedpairs tests and sex differences were analyzed with the Mann–Whitney U test (Siegel and Castellan 1988).

Because there was no effect of time of day on relative energygain of the animals, the mean of morning and afternoon feedingobservations was used in the following analyses. Under dispersedfood distribution almost all food was eaten within 20 min. There-fore, we used this 20-min period as a baseline of scramble com-petition for further analyses and divided the 60-min observationsession of feeding under clumped food distribution into three 20-min observation blocks (0–20 min, 21–40 min, and 41–60 min).During a feeding session under clumped food distribution, malesand females obtained on average during the first two 20-min blocksmore than 95% of their total food intake. Therefore, the last 20-min block under clumped food distribution was ignored in theanalyses (see Stahl 1998 for details).

Means are reported with standard errors throughout this arti-cle. Only two-tailed tests were used. A null hypothesis was rejectedat an a-level of 0.05 with the exception of dependent samples ofmales. Here, a null hypothesis was rejected at an a-level of 0.07because of the small sample size.

Results

The overall female mean relative energy gain within60-min feeding sessions did not differ between the twofeeding conditions (F(1,8)=0.046, P=0.836, n=10).Animals were foraging longer under clumped (‡50 min)than under dispersed food distribution where basicallyall food was eaten within 20 min.

Table 2 Categories for interindividual distances between adultfemales and adult males

Category Interindividualdistance

Area (m2) Weighting factor(1/area*p)

1 £ 0.5 m (arm’sreach)

0.785 4

2 0.5 m to £ 1 m 2.36 1.333 1 m to £ 2 m 9.42 0.334 >2 m 0

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Access to food

Figure 1 shows the relationship between female rankand food intake success, measured as relative energygain, under clumped and dispersed food distribution.Under clumped food distribution, high-ranking femalesgained more relative energy during the first 20 min offeeding sessions than lower-ranking females (Fig. 1a,

Table 3). Lower-ranking females could not completelycompensate for their deficit at a later time, resulting in atendency for high-ranking females to be more successfulin obtaining relative energy during a total 60-min feed-ing session (Fig. 1b, Table 3).

Similarly, high-ranking females spent more timewithin the feeding area during the first 20 min underclumped food distribution (r=0.64, P<0.05, n=10;Fig. 2a), and time spend within the feeding area waspositively associated with relative energy gain (r=0.84,P=0.005, n=10; Fig. 2b). There was no relationshipbetween time spent in the feeding area and rank duringthe second or third 20-min block (21st–40th min:r=)0.315, P=0.375; 41st)60th min: r=0.018, P=0.960, n=10) and overall, high-ranking females tendedto spend more time within the feeding area during acomplete feeding session under clumped food distribu-tion (r=)0.587, P=0.074, n=10). Under dispersed fooddistribution there was at no time a correlation betweenfemale rank and relative energy gain (Fig. 1c, Table 3)or time spent in the feeding area (0–20th min: r=)0.098,P=0.787, n=10).

Agonistic behavior

Although female feeding success correlated positivelywith rank only during the first 20 min under clumpedfood distribution, there was no difference in aggressiveand submissive interaction rates among the femalescompared with under dispersed food distribution orcompared with the second 20 min under clumped fooddistribution (Figs. 3, 4). Only during the first 20 minunder clumped food distribution were rates of maleaggression toward females substantially higher thanrates of aggression between females. During this time,males showed the highest levels of aggressive behaviortoward females compared to other observation periodsunder clumped and dispersed food distribution (Fig. 3).Similar patterns were observed for female submissivebehavior rates toward males (Fig. 4). During feedingunder both food distributions no coalitions betweenfemales were observed.

Fig. 1a–c Correlation between female rank and relative energygain during the first and second 20-min block under clumped fooddistribution (a, b) and the first 20 min under dispersed fooddistribution (c). Relative energy gain is standardized by the mean ofeach group (n=10)

Table 3 Correlation between female rank and standardized relativeenergy gain during different observation blocks under clumped anddispersed food distributions (Pearson product–moment correlation,n=10)

Period r P

Clumped food distributionTotal (0–60th min) –0.61 0.0590–20th min –0.664 0.03621–40th min –0.244 0.49741st–60th min 0.111 0.760

Dispersed food distribution0)20th min 0.380 0.2760–10th min 0.310 0.386

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Feeding area

Under clumped food distribution females’ mean stay inthe feeding area during the first and the second 20-minblock did not change (Fig. 5). Males stayed longerduring the first 20-min block than during the second20-min block under clumped food distribution (Wil-coxon matched pairs test: Z=1.826, P<0.07, n=4).During this time period males spent more time thanfemales within the feeding area (Mann–Whitney U test:Z=)2.404, P=0.016, nmales=4, nfemales=10). At leastone of the two males stayed within the feeding areaduring more than 80% (group S1: 80.9%; group S3:82.2%) of the time (Fig. 5) and here mainly directly atthe food box. During the remainder of this time period,usually at least one of the males was close by thefeeding area. During this first 20-min block, femalesspent most of their time within the feeding area with atleast one male (Fig. 6; two-way ANOVA with repeatedmeasurements: F(1,8)=11.735, P<0.009). During thesecond 20-min block, males were less often within thefeeding area, and females usually fed when males werenot present in the feeding area (Fig. 6; two-way

ANOVA with repeated measurements: F(1,8)=25.685,P<0.001).

Male–female relations

Direct competition between the sexes occurred, therefore,mainly at the beginning of the feeding session. During thistime period, high-ranking females stayed in closer prox-imity to the males (r=)0.78, P=0.007; Fig. 7a). In bothgroups, it was mainly the dominant female who sat andfed especially with the alpha male directly at the food box(Fig. 8a, b). Taking proximity into account, high-rankingfemales experienced less aggression from and showed lesssubmissive behavior toward males than did low-rankingfemales (aggression received: r=0.87, P=0.001; Fig. 7b;submission: r=0.78, P=0.008; Fig. 7c). Females whostayed closer to the males stayed longer within the feedingarea (Fig. 9a; Pearson’s correlation: r=0.940, P<0.001)and gained more relative energy (Fig. 9b; r=0.867,P<0.001). Proximity to males thus accompanies females’access to food under clumped food distribution.

Fig. 2 a Correlation between female rank and standardized timespent in the feeding area during first 20 min under clumped fooddistribution. b Correlation between standardized time spent in thefeeding area and standardized relative energy gain during first20 min under clumped food distribution. Data are standardized bythe mean of each group (n=10)

Fig. 3a, b Female (a) and male (b) mean aggressive behaviortoward adult females under clumped (cl) and dispersed (di) fooddistribution during the first (cl 0–20) and second (cl 21–40) 20-minblock under clumped food distribution and the first 20-min block(di 0–20) under dispersed food distribution. Asterisk *P<0.05(P<0.07 for dependent samples with males). Statistical test forfemale and male aggressive behavior as follows. Clumped0–20th min versus dispersed 0–20th min: males (Wilcoxon test):T=0, Z=1.83, P<0.07, n=4; females (two-way ANOVA withrepeated measurements):

Factor df F P-level

Group 1,8 2.949 0.124Distribution 1,8 0.251 0.630Group·Distribution 1,8 1.042 0.337

and clumped 0–20th min versus clumped 21st–40th min: males(Wilcoxon test): T=0, Z=1.83, P<0.07, n=4; females (two-wayANOVA with repeated measurements):

Factor df F P-level

Group 1,8 1.004 0.346Distribution 1,8 0.311 0.592Group·Distribution 1,8 0.003 0.955

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Grooming relations

Females did not groom males longer during non-feedingtimes following feeding sessions under clumped com-pared to under dispersed food distribution (Table 4).High-ranking females groomed the a- and b-maleslonger than lower-ranking females independent of thefood distribution (Table 5). Males hardly groomedfemales during non-feeding observations under bothfood distributions (Table 4). The dominant female ofboth groups was in no case recipient of the mostgrooming by males.

Discussion

In this study, access to food among adult female man-gabeys was rank dependent under clumped but notunder dispersed food distribution, as the model of vanSchaik (1989) predicts for species’ everyday behavioradapted to contest food competition and as has beenshown for many FB species (Sterck et al. 1997): High-ranking female mangabeys stayed longer within thefeeding area and closer to the preferred food site thanlower-ranking females, thereby obtaining more food.Experimental studies on two captive groups of NFBspecies did not reveal better feeding success of high-ranking females under either clumped or dispersed fooddistribution (Presbytis obscurus: Kerscher 1991; Papiohamadryas: Gore 1993; Zinner 1993).

Contrary to the predictions derived from the vanSchaik model, females’ differential feeding success at therestricted food resource was not accompanied by directagonistic competition between females: there was nodifference in female aggressive and submissive behaviorbetween feeding under clumped and dispersed fooddistribution. If females were trying to restrict otherfemales’ access to food, agonism levels should be higherunder a clumped than under a dispersed food distribu-tion, as has been described in several FB species (e.g.Cebus capuchinus: Phillips 1995a; Cercopithecus (Chlor-ocebus) aethiops: Pruetz and Isbell 2000;Macaca fuscata:Mori 1977; Saito 1996; M. mulatta: Belzung andAnderson 1986; Brennan and Anderson 1988; M. radi-ata: Boccia et al. 1988; P. anubis: Barton and Whitten1993).

Similarly to our study, in two captive studies of NFBspecies, agonism rates between females did not differduring feeding under clumped and dispersed food dis-tribution (Presbytis obscurus: Kerscher 1991; Papiohamadryas: Zinner 1993). Females of both speciesmaintained their scramble competitive social systemunder artificial clumping as expected for NFB speciesadapted only to non-monopolizable food resources. In afield study, Sterck (1995) showed that the displacementrates between females of the NFB Thomas langurs weresimilarly high to those of the sympatric, FB long-tailedmacaques (see also Sterck and Steenbeck 1997). How-ever, aggression rates in female langurs did not differ

when feeding on leaves compared with feeding on fruits,which were expected to induce scramble and contestcompetition, respectively. The aggressive and submissivebehavior rates between female sooty mangabeys underclumped compared with under dispersed food distribu-tion, therefore, resembled those of several NFB species.

The comparison of agonistic behavior between twotime periods under clumped food distribution showedthat aggressive and submissive behavior rates betweenfemales were not higher during the first time periodwhen feeding success was rank related and individualvariance was larger. Because mean time that femalesstayed within the feeding area during the two timeperiods did not differ, higher rates of aggressive andsubmissive interactions were expected during the firsttime period if females are adapted to contest competi-tion (cf. Janson and van Schaik 1988; van Schaik 1989).

Fig. 4a, b Female submissive behavior toward females (a) andmales (b) during the first (cl 0–20) and second (cl 21–40) 20-minblock under clumped food distribution and the first 20-min block(di 0–20) under dispersed food distribution. Asterisks **P<0.01.Statistical tests for female submissive behavior as follows (two-wayANOVAs with repeated measurements). Clumped 0–20th minversus dispersed 0–20th min:

Factor df F P-level

Toward femalesGroup 1,8 4.480 0.067Distribution 1,8 3.190 0.112Group·Distribution 1,8 5.786 0.043

Toward malesGroup 1,8 0.029 0.868Distribution 1,8 16.91 0.003Group·Distribution 1,8 0.127 0.731

and clumped 0–20th min versus clumped 21st–40th min:

Factor df F P-level

Toward femalesGroup 1,8 2.403 0.150Distribution 1,8 3.412 0.102Group·Distribution 1,8 0.389 0.550

Toward malesGroup 1,8 0.398 0.547Distribution 1,8 17.941 0.003Group·Distribution 1,8 0.081 0.783

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Contest competition can be mediated not only byovert aggressive and submissive interactions but also byspatial deployment mechanisms, especially in systemswith decided dominance relations. Subordinate animalscan avoid overt costly conflicts over restricted resources(food or safe positions) by occupying locations awayfrom the dominant animals and the contested resourceas has been described for several FB species (e.g. Cebusapella: Janson 1990; C. olivaceus: Robinson 1981;Cercocipethecus aethiops: Whitten 1983; Macaca fascic-ularis: van Noordwijk and van Schaik 1987; M. fuscata:Saito 1996; M. mulatta: Belzung and Anderson 1986;Papio anubis: Barton 1993; P. cynocephalus: Collins1984). However, only in one study by Whitten (1983 onC. aethiops) was rank-dependent access to clumped foodpatches maintained by spatial avoidance without a pre-vious increase of aggression.

In our study, food was presented at only one place in aspatially restricted environment. Low-ranking animalscould not avoid conflicts by feeding at a different, less-profitable or less-safe patch, as observed by Whitten(1983) in female vervet monkeys or by Saito (1996) inJapanese macaques) or by even foraging outside the maingroup (e.g. M. fascicularis: van Noordwijk and vanSchaik 1987). Furthermore, in this study the amount offood was restricted to the amount they actually needed(no surplus). Because both mangabey groups were feed-ing more during ad libitum feeding than during theexperimental phase, low-ranking animals could not avoiddominant animals at the food resource by feeding at alater time of day when higher-ranking animals were fin-

ished feeding. This has been seen, for example, in vervetor capuchin monkeys (Whitten 1983; Phillips 1995b).

It is, therefore, unlikely that the differences infemales’ feeding success at the restricted food resourcewere mediated by subtle competitive mechanisms amongthe female mangabeys without an initial increase ofaggression, especially since the same females did notavoid the high level of aggression of the larger malesduring the same time period.

A comparison of wild and provisioned Japanesemacaques by Hill and Okayasu (1995, 1996) showed thatprovisioning groups with food induces closer proximityamong females. Closer proximity increases the chancesof having potential allies around. Alliances were, there-fore, more profitable and occurred more often thanamong females in wild groups. The authors assumedthat the youngest ascendancy hierarchy in female ma-caques might be a result of a high level of opportunityfor effective alliances in provisioned or captive groups.In our study both groups of mangabeys should thereforeshow more female–female alliances under clumpedfood distribution if females are adapted to contest

Fig. 5 Mean time (and standard error) females spent in the feedingarea in comparison to total time at least one male stayed within thefeeding area during the 0–20th min and the 21st–40th minobservation block under clumped food distribution. Statistical testfor the effect group membership and 20-min blocks on time femalesstayed in the feeding area during feeding session under clumpedfood distribution as follows (two-way ANOVA with repeatedmeasurements):

Factor df F P-level

Group 1,8 0.720 0.42120-min block 1,8 0.280 0.611Group·20-min block 1,8 0.026 0.875

Fig. 6 Mean relative number of scans females of group S1 and S3spent in the feeding area with or without a male present in thefeeding area during the 0–20th-min and the 21st–40th-minobservation block of a feeding session under clumped fooddistribution (n=10). Asterisks **P<0.01; ***P<0.001. Righty-axis Mean time spent per 10 min estimated from instantaneousscan samples (seconds/10 min). Statistical test for effect of groupmembership and presence of males in the feeding area on timefemales spent in the feeding area, with and without males in thefeeding area (two-way ANOVA with repeated measurements) asfollows. Clumped 0–20th-min block:

Factor df F P-level

Group 1,8 0.016 0.903Males present 1,8 11.735 0.009Group·Males present 1,8 0.048 0.832

and clumped 21st–40th-min block:

Factor df F P-level

Group 1,8 0.291 0.604Males present 1,8 25.685 <0.001Group·Males present 1,8 0.127 0.731

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competition. However, during feeding under both fooddistributions there were no female alliances observed.

Concluding, different competitive feeding situationsamong female mangabeys did not result in changes ofthe agonistic level. Access to food in female mangabeyswithin a social group seems not to be mediated by direct

competition between females as is the case in FB species.Although there is a strict dominance hierarchy amongthe female mangabeys, the relationships between themappear to be egalitarian in the context of food compe-tition as defined by de Waal and Luttrell (1989). Com-petition for food between the female mangabeys can bedescribed as mainly of the non-contest type and cannotaccount for the rank-related differences in feeding suc-cess. The van Schaik model does not describe thiscompetitive social system.

Male influence on female feeding success

Rank-related feeding success among the studied adultfemales, however, was associated with a high level ofmale aggression and occupation of the food resource byone of the males. During this time period underrestricted feeding conditions males were most aggressivetoward adult females (and other non-adult groups)

Fig. 7a–c First 20-min block under clumped food distribution:correlation between female rank and (a) standardized proximityindex toward both males, (b) aggression received from males/proximity index under clumped food distribution, and (c) submis-sion shown toward males/proximity index

Fig. 8a, b Time individual females of group S1 (a) and group S3(b) stayed simultaneously with the a- or b-male at the food boxduring the first 20 min of a feeding session under clumped fooddistribution (curves fitted by method of least square smoothingprocedure). Male 1 a-male; male 2 b-male

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and, correspondingly, females’ rates of submissiveinteractions toward males were highest. Similarly, maleaggressive behavior was highest during the time periodsunder restricted food resources when they stayed lon-gest at the food resource and obtained the most food.

Females were, therefore, more affected by male thanby female direct agonism under restricted food re-sources.

Males restricted but did not fully monopolize accessto food. Females’ access to food seems to be restricteddifferentially by the males: high-ranking females wereless aggressed by the males and showed less submissivebehavior toward them. Because of closer proximity tomales, these females stayed longer within the feedingarea and closer to the food box, which allowed betteraccess to food.

Female sooty mangabeys showed predictable domi-nance effects in feeding success similar to FB species butdifferential access to the food resource and feedingsuccess among females seem to be determined by a lowercompetitive tendency of dominant males toward higher-ranking females. Males selectively expressed ‘‘socialtolerance’’ (sensu de Waal 1986, 1989) toward higher-ranking females.

In addition to dominance, social tolerance candetermine feeding success and according to de Waal(1986, 1989) social tolerance opens an alternative routefor subordinate animals to gain access to food or otherresources. Being tolerated by a particular dominant malemight give a female higher payoffs than trying to com-pete with other females. On an ultimate level, it could bea strategy for female primates to become tolerated bydominant males instead of competing with other femalesas van Schaik assumes in his model.

In both groups, the dominant female showed strongassociations especially with the dominant male. Amongthe females, the dominant female almost exclusivelystayed and fed together with the dominant male at thefood box. This strong association can be regarded as a‘‘special relationship’’ (cf. Smuts 1985). Therefore,among female mangabeys in this study the special valueof being dominant is that her close association with themale can provide her priority of access to food overadult females, the second-ranking male, and all othermembers of the group.

Male–female associations were observed in wild sootymangabeys (Range 1998). Although sooty mangabeys inthe wild do not exhibit such restricted food resources aspresented in this study, they feed on patches, which areunlikely to accommodate the whole group (Range andNoe 2002). A female’s association with a dominant male

Table 4 Mean duration (and standard error) of female–male andmale–female grooming sessions during non-feeding observationsunder clumped and dispersed food distribution (seconds/10 minper individual)

Grooming session Clumped fooddistribution

Dispersed fooddistribution

Females groominga

a-male 19.7 (11.67) 26.3 (9.82)b-male 27.6 (11.61) 23.6 (10.95)

Females groomed bya-male (S1) 1.6 (1.57) 4.3 (1.95)b-male (S1) 1.0 (0.66) 0.4 (0.27)a-male (S3) 5.2 (2.39) 4.6 (1.81)b-male (S3) 0 0

aStatistical test for females grooming the a- and b-male (non-feeding observations under clumped vs. under dispersed food dis-tribution; two-way ANOVA with repeated measurements): factorGroup: df=2,7, F=0.861, P=0.124; factor Distribution: df=2,7,F=0.255, P=0.630; factor Group·Distribution: df=2,7, F=0.332,P=0.337

Fig. 9a, b Correlation between standardized proximity indextoward both males and (a) standardized time females spent in thefeeding area and (b) standardized female relative energy gainduring first 20 min under clumped food distribution. Time data arestandardized by the mean of each group (n=10)

Table 5 Correlation between female rank and time spent groomingthe a- and b-male, respectively, of each group during non-feedingtimes under clumped and dispersed food distributions (Pearsonproduct–moment correlation, n=10; time standardized by thegroups’ mean)

Females grooming Clumped fooddistribution

Dispersed fooddistribution

r P r P

a-male –0.791 0.006 –0.645 0.044b-male –0.638 0.047 –0.670 0.034

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can, therefore, be an advantage for better access to afood patch and for feeding unhindered within it.

Most primate studies on food competition havefocused only on female–female interactions and have nottaken male influences on differences in females’ feedingsuccess into account. However, a comparable pattern ofcompetitive behavior in clumped food situations asshown in this study was observed among wild brownand white-capped capuchin monkeys (Cebus apella:Janson 1984, 1988, 1990; C. capucinus: Fedigan 1993;Rose 1994). While foraging, males were more aggressivethan females toward females, and males’ agonismsadversely affected females’ foraging success. The domi-nant male restricted access to the best feeding sites whereonly the dominant female and her offspring were toler-ated. In some clumped high-quality food patches, wholefruit trees were monopolized by this pattern (C. apella:Janson 1988, 1990). In several other primate species, itwas also noted that adult females sitting close to theirmale ‘‘friend’’ (sensu Smuts 1985) had better access torestricted food resources than higher-ranking animals(M. fuscata: Takahata 1982; P. anubis: Smuts 1985;M. mulatta: Chapais 1986).

Recently, the influence of adult male primates onfemale social relationships has been incorporated intothe van Schaik model (van Schaik 1996; Sterck et al.1997) but only male sexual coercion (Smuts and Smuts1993), including male infanticidal behavior, was con-sidered as a major ultimate factor. Sterck et al. (1997)suggested that in NFB species the threat of infanticideby new immigrating males may force females to leave thegroups (e.g. mountain gorillas: Watts 1990; Thomaslangurs: Sterck and Steenbeck 1997). Male infanticidalbehavior after joining a new group or after a rankreversal may further explain the formations of male–female special relationships after mating because of maleprotection of the infant (van Schaik and Dunbar 1990;Smuts and Smuts 1993; van Schaik 1996). This studydemonstrates another possible effect of males on femalesocial relationships that is not considered in van Schaik’smodel: the establishment of a special relationship with ahigh-ranking male can be a strategy to get better accessto food. Competition for access to restricted foodresources would be mediated via the males and not bydirect competition between the females. This aspectshould be considered in future (field) studies and mayneed to be integrated into current models of the evolu-tion of social systems in primates.

Infanticide or predation pressure is likely to act onthe establishment of this social system as well. A female(and her offspring) may further benefit from a male’sclose presence by getting better access to safe positionsagainst predators or by protection against potentialinfanticidal males (as was observed by Busse and Gor-don (1983, 1984) in captive sooty mangabeys). Thiswould further enhance the power of male–female rela-tionships. Helping and protecting his most likely infantas well as establishing and maintaining access to mating

partners would explain why a male should have aninterest in such a relationship.

If access to food (or safe position) is not mediated bydirect competition between females as proposed by vanSchaik but by the differential tolerance of males towardfemales during foraging, females’ strategies to improvefeeding success should be aimed at establishing andmaintaining a relationship with a male. Grooming isgenerally regarded as a means to establish affiliativecontact and to maintain social relationships (Boyd andSilk 1997). In this study, females groomed males moreoften than vice versa during non-feeding times and high-ranking females groomed the two males in each groupmore often than did the low-ranking females. Therefore,female mangabeys, especially high-ranking ones, seem toinvest in a good relationship with males.

The effect of males’ presence in groups on females’competitive system has been hardly looked at, possiblybecause of the popular view that females competemainly for food (Hemelrijk and Luteijn 1998). How-ever, there are growing indications and observationsthat female primates compete for males (e.g. Kummer1968; Smuts 1987; Zinner et al. 1994; Kuster and Paul1996; Hemelrijk and Luteijn 1998; Palombit et al.2001). In this study it was occasionally observed that ahigher-ranking female displaced another female whowas grooming a male at that time and groomed themale herself afterward. Due to the small number ofobservations during focal animal sampling of suchagonistic interactions, a quantitative analyses was notpossible. Disturbing the grooming interaction might beused to prevent the lower-ranking female from estab-lishing a relationship with a dominant male. A quan-titative analysis of grooming competition especiallyduring times of instability of adult and subadult femaledominance relationships (Gust 1995) or introductionsof new males would be of special interest to get furtherinformation on female competition over access tomales.

Summarizing, this study suggests researchers shouldconsider a further role of males in current socioecolog-ical models of the evolution of primate social systems. Itdemonstrates that future primate studies on femalecompetition for access to food should not be analyzedseparately from male influences on females. This aspectis neglected in most studies on food competition infemale primates.

Acknowledgements We thank Debbie Gust and Tom Gordon formaking it possible to study the mangabeys at the field station of theYerkes Regional Primate Research Center. Many thanks are owedto both for their support and help. We are grateful to the caretakersof the field station for their valuable help and cooperation, and toFilippo Aureli, Joachim Burghardt, Joanna Fietz, Len Thomas,Dietmar Zinner, and three anonymous referees for their helpfulcomments on the manuscript. Last we wish to thank Prof. H-JKuhn for his support. This study was supported by the DeutscherAkademischer Austauschdienst (512 402 575 3) and DeutscheForschungsgemeinschaft (KU131/13-1). Animal maintenance wassupported by a Yerkes NIH base grant.

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