Isbell 1994 Evol Anthro

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ARTICLES Evolutionary Anthropology 61

Predation on Primates: Ecological Patterns andEvolutionary ConsequencesLYNNEA. ISBELL

It has long been thought that predation has had important ecological and evolu-tionary effects on primates as prey. Predation has been theorized to have been amajor selective force in the evolution of hominids. In modern primates, behaviorssuch as active defense, concealment, vigilance, flight, and alarm calls have beenattributed to the selective pressures of predation, as has group living tself. It is clearthat primates, like other animals, have evolved ways to minimize their risk of pre-dation. However, the extent to which they have been able to do so, given otherconstraints of living such as their own need to acquire food, has not yet beenresolved. Perhaps most hotly debated is whether predation has been the primaryselective force favoring the evolution of group living n primates. Part of the difficultyin resolving the debate lies in a paucity of direct evidence of predation. This isregrettable yet understandable since primatologists, by definition, focus on the studyof primates, not predators of primates (unless hese are also primates). Systematicdirect evidence of the effects of predation can best be obtained by studying preda-tors that are as habituated to observers as are their primate prey. Until this is done,we must continue to rely on opportunistic accounts of predation and predationattempts, and on systematically obtained indirect evidence. Such data reveal sev-eral interesting patterns: 1) although smaller primates may have greater predationrates than larger primates, even the largest primates are not invulnerable to preda-tion; 2) the use by primates of unfamiliar areas can result in higher predation rates,which might be one pressure favoring philopatry, or site fidelity; 3) rboreal primatesare at greater risk of predation when they are more exposed (at forest edges andtops of canopies) than in more concealed locations; 4) predation by mammaliancarnivores may often be episodic; and 5) terrestrial primates may not experiencegreater predation than arboreal primates.

Predation on primates has long oc-cupied a place in the minds of natural-ists. Early in this century, Fitzsimons2described the behavior of vervet mon-keys (Cercopitkecus aetkiops) in thepresence of leopards (Panthera pa rdus) :

When a leopard is discovered by atroop of Vervet Monkeys they invari-

Lynne lsbell is an assistant professor ofanthropology at Rutgers University. Trainedin animal behavior, she focuses onquestions involving the evolution andmaintenance of sociality, particularly inprimates. She recently received fundingfrom the National Science Foundation toinvestigate the ecological determinants ofvariation in social relationships in vervetsand patas monkeys in Laikipia, Kenya.Key words: episodic predation, philopatry,resource competition, group living, predation rate

ably desert the locality, for they a rewell aware tha t otherwise it is but amatter of time for the whole of thetroop to disappear one by one into thecapacious stomach of their arch-en-emy, which never neglects an oppor tu-nity of reducing their numbers an dthus fulfilling its mission in life.With the application of systematic

science to natural history, we nowknow that vervets are less likely toleave the area when they see a leopardthan to flee up the nearest tree andgive alarm calls specific to leopardsand other terrestrial carnivore^.^,^Flight and alarm-calling ar e just twoof the many behaviors that primateshave at their disposal to avoid preda-tion. In 1987, Cheney and Wrangham5provided an exemplary review of pre-

dation on primates. Since then, ourknowledge of this subject has steadilyincreased. In this review, I will not tryto cover again all of the informationprovided by Cheney and Wrangham,which I recommend as companionreading. Instead, I will attempt tobring together recent data and ideasabout predation on primates in thelight of previous information.

The kinds of anti-predator strate-gies available to primates depend, inpart, on their body sizes relative tothose of their predators.5 Small pri-mates can conceal themselves; largerprimates may mob predators, with orwithout physical contact. All primatesexcept the largest, Gorilla gorilla, sleepoff the ground in nests, holes, or trees,or on cliffs. Sleeping in trees and othershelters, which undoubtedly reducesthe risk of predation from strictly ter-restrial predators, probably evolvedtoserve this purpose. Direct observa-tions of avoidance, escape, and defen-sive behaviors by primates in thepresence of predators suggest thatpredation has been an important se-lective force in the behavioral evolu-tion of primates (reviewed in Cheneyand Wranghams; see also Table 1) .Pri-mates are not exceptional in this; suchbehaviors are common in most, if notall, animals.PREDATION AND THE EVOLUTIONOF GROUP LIVING IN PRIMATES

Primates are among the most socialorders of animals: at least 73%of spe-cies (94 O f 129) are known to travelwith one or more adult conspecifics.6Until recently, it was assumed thatpredation was the major selectiveforce favoring group living in pri-mates. The assumption was that liv-ing in groups reduces the risk ofpredation by increasing vigilance and


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TABLE 1. ContinuedCharacteristic Supporting Evidence ExamDles CommentsSuggested Patternsof Predation:Human presence reduces Inferred

Dredation

Males at greater risk inferred

Predation limits populations inferredSmaller primates at greater risk Inferred

Correlated with number of es-trous females of predator

Terrestrial primates at greater riskInferredSuggested

Vervets Predation negatively correlatedwith spatial and temporalvariation in human presence

Sex ratio often skewed towardadult females; males havehigher mortality than femalesPredation high with no evidence

of food competitionSmaller primates may be

vulnerable to greater numbersof predators and cannotactively defend themselves

Male chimpanzees provide meatto estrous females

Evidence not convincing

Species with male dispersal

Red coiobusMany strepsirhines, callitrichids

Red colobusBaboons, vervets. patas

flight distance and by decreasing theprobability that any particular individ-ual would be killed during a predationevent. Alexander suggested that onlythis reduction in the risk of predationcould outweigh the inevitably highercosts of food competition resultingfrom living in close proximity to con-specific^.^

A number of studies have providedevidence that intragroup competitionincreases as group size increases.a12There isalsoevidence that p u p sprovidean advantage in avoiding or minimizingpredation. Among wedgecapped capu-chins (Cebus olivaceu s) and vervets, forexample, large groups show higherlevels of vigilance than do smallgroup^.^^^^^ Among long-tailed ma-caques (Macaca fasc icularis) , largegroups detect human potential preda-tors earlier than do small ones. Thelarge groups also spend more time lowin the canopy where, presumably, theyare at greater risk from terrestrialpredators than they would be at higher1e~els.I~owever, it is not yet clearwhether the avoidance of predation isa primary cause or a secondary conse-quence of living in groups (see Box 1).

Wrangham challenged the notionthat predation avoidance is the solefactor favoring group living, arguingthat although living in groups neces-sarily increases competition for foodwithin the group (intragroup competi-tion), this cost is outweighed, not pri-marily by decreased predation, but bygreater advantages in competition

against solitary individuals andsmaller groups for food (intergroupcompetition).16 Predation avoidanceand intergroup competition are notthe only explanations for the evolutionof group living-for example, im-proved foraging efficiency could alsofavor gro up l i ~ i n g . ~ ~ , ~ *evertheless,Wrangham's seminal paper polarizedthe views of some primatologists a sthey attempted to exclude either pre-dation avoidance or intergroup com-petition as the primary selective forcefavoring group living.

In one such attempt, van Schaik'gsuggested tha t the two selective pres-sures predict different birth rates ingroups of different sizes. He arguedthat if predation is the primary selec-tive force favoring group living, thenbirth rate, measured by numbers of in-fants per adult female, should de-crease a s group size increases, becausefood intake decreases with group size.On the other hand, Schaik contended,if intergroup competition is the pri-mary selective force favoring groupliving, birth rate should first increaseas group size increases and then de-crease when the group becomes verylarge because intragroup competitionfor food eventually outweighs the ad-vantage of being in the largest groups.Using a sample of 14 species, mostwith single-male, multi-female group-ing patterns, he found that the patternof birth rates fit closely with his pre-diction derived from the predation hy-pothesis. However, much rests on

whether the underlying assumptionsare reasonable. For instance, social in-stability or high rates of infanticide inlarge single-male, multi-female groupsmight cause the same pattern predictedby the predation hypothesis. 11.20 Twolong-term studies of species with multi-male, multi-female grouping patternsfound that female reproductive successincreased with group size, a result thatis consistent with the intergroup compe-tition hypothesis.21z22Isbell et al.23 suggested that invervets the behavior of juveniles couldbe used to distinguish between the ef-fects of predation avoidance and inter-group competition in maintaininggroups as cohesive units. We consis-tently observed that vervet groups de-clining in size persisted as separateunits as long as there were at least twoadults in each group. Almost immedi-ately after losing its penultimate adul t,however, each group fused with aneighboring one. The number of juve-niles did not appear to influence thetiming of group fusions. Juveniles areactive participants in predator detec-tion, but not in aggressive intergroupencounters. This suggests that mini-mum group size in vervets is a limita-tion set by successful intergroupcompetition rather than by predatordetection o r avoidance (see Box 1).On an ecological time scale, the in-fluences of predation and food compe-tition may, in fact, be nearlyinextricable. For example, decliningfood resources caused large groups of


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64 Evolutionary Anthropology ARTICLES

The Evolutionof Group Size and theEvolutionof Group LivingWhat selective forces are responsible for the evolution and m aintenance ofgroup living in animals? Tests of hypotheses addressing this question haveexamined he advantages and disadvantages of m odern variation n group size,and therefore address the evolutionary maintenance of group size and, by ex-tension, group living. There are two ways in which these are risky tests of theconditions favoring the initial evolu tion of group living.First, the selective factors that maintain a trait are not nece ssarily the onesthat were responsible or its 0rig ina tion .'8.~ ~or examp le, there is evidence that,in several primate species, ndividuals n large groups benefit n both intergroupcompetition and predator avoidance. However, this ev idence does not neces-sarily identify either benefit as the prima ry selective orce on grou p size or grou pliving. Even negative evidence for one selective force nee d not eliminate it as athe initial cause: the conditions that existed at the time the adaptation (groupliving) first arose m ay not be the sam e as the conditions under which currentselective factors are being ested.74 uch historicaleffects may include changesin predation risk, food abundance, or food distribution. They may also include

group size itself.This leads to the secon d point. Group living evolved when the first individualsof an evolutionary lineage ceased to live alone, probably through m others' tol-erance of their daughters. In any case, the initial transition was almost certainlyfrom living solitarily to living in groups of two . Ho wever, most tests of the advan-tages of grou p living are not direc ted at this thresho ld of so ciality. The s electiveforces that first favored living in pairs over living alone n eed not h ave been thesame selective orces that now favor a group of twenty o ver a group of ten. Mo stsocial primates live in groups far above this threshold, only rarely providingopportunities o examine behaviors at minimal group size, and even then, underextreme and possibly anomalous condition^.^^ Better tests m ight be carried outamong primates in which group sizes are characteristically small, such as cal-litrichids and many prosim ians. Thus far, such tests are lacking. The fission-fu-sion societies of chimpan zees m ay provide some insight here . Fusion amongchimps is often associated with intergroup co nf l i~ t. ~ 5, ~6owever, mass at-tacks on predators are also observed.35We may still be left with multiplesupportable hypotheses. TP Young

vervets to supplant small ones, and allgroups moved into areas where theybecame more vulnerable to preda-tion.24 Similarly, a change in predationrate can affect food competition. Ifpredation increases to a level that low-ers prey population size it could in-crease the availability of food for thoseremaining and , presumably, decreasefood Competition. On the other hand,a decrease in predation and the sub-sequent increase in the prey popula-tion could increase food competitionwithin i t .

A s another example of the codepen-dence of predation and food competi-tion, vigilance is often inverselyrelated to time spent f ~ r a g i n g . ' ~ , ~ ~orindividuals in smaller groups, greaterdemands on their time for vigilance

could reduce their food intake and,therefore, their reproductive successrelative to that of individuals in largergroups (see also Janson26). n groupsof all sizes, decreased food availabilitycould increase time members spendforaging and decrease their vigilance,leading to an increase in predation onthem. Even within groups, individualsmay face different trade-offs betweenvigilance and food intake. In a study ofbrown capuchins (Cebus apella), forexample, dominant adults foraged inthe most productive areas, while sub-ordinate adults foraged in sub-opti-ma1 areas both for food intake andvigilance. Juveniles, on the other handforaged in subo ptimal areas wherethey also spent less time in vigi-l a n ~ e . ~ 5 , * ~

Figure 1 suggests that group livingcould have evolved by predation alone(pathway I ) , resource competitionalone (pathway 2), or through a com-bination of predation and resourcecompetition (pathway 3) . Given theinteractive effects of predation andfood competition, debate about theirrelative influences on group livingshould continue to flourish until moredata have become available and addi-tional creative tests have been devel-oped, if not for even longer (see Box 1).Most valuable will be investigations hatdispassionately consider multiple cau-sation.'DIFFICULTIES IN DOCUMENTINGPREDATION ON PRIMATES

No tests of the effects of predationand food competition have directlymeasured the intensity of predation. Ithas been relatively easy to documentthe advantages of large groups in in-tergroup competition in various spe-c i e ~ . ~ ~ , ~ ~ - ~ ~ , ~ ~t has been more difficultto document predation. There are sev-eral reasons for this.

First, predation rates are often verylow. Based on extrapolation from sus-pected number s of predations,Cheney and Wrangham5 estimatedthat the median yearly predation ratein 24 populations of primates wasabout 3% (range, O->l5%). Second,even when predation rates are high,individual events often happen soquickly that there is little chance of ob-serving them. For example, in a recentaccount of lion predation on a savan-nah baboon (Papio ynocephalus a m -bis), he entire episode took only oneminute.29Third, many predators, suchas barn owls (Tyto alba)3O and leop-a r d ~ , ~ ~unt at night when observersare not usually present. Fourth, ob-servers may, in fact, inhibit the hunt-ing activities of predators. In the firstsix months of a recent study of vervetmonkeys, Isbell and Y0ung3~ oundthat leopard predation on vervets wassignificantly lower when observerswere present in the study area thanwhen they were absent. A s the studyprogressed, this difference disap-peared. Observations of one leopardincreased, suggesting that it was be-coming habituated to the observersand less wary of hunting vervets whileobservers were in the area. Nonethe-


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66 Evolutionary Anthropology ARTICLES

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D i s t a n c e f r o m h u m a n s e t t l e m e n t (km) Group sizeFigure 3. The reiationship between estimated predation rate and distance to human habitat ion (a) and group size (b) across five groups of vervetmonkeys in Amboseli, Ken ~a .3~

ject to predation adds credence to thenotion that predation could have beena strong selective force on early homi-nids.'2 ) It has long been hypothesizedthat animals are more vulnerable topredation when they are in unfamiliarareas.37.38 Support for this notion hasnow been obtained from vervets. As aresult of natural habitat change in Am-boseli National Park, Kenya, entirevervet groups gradually shifted theirhome ranges into areas they had notpreviously inhabited.24Some of thesegroups eventually became so smallthat the remaining members aban-doned their home ranges and immi-grated into groups with differentranges.39In both situations, vervetsbegan using areas that were unfamil-iar to them. During this time, manyvervets disappeared, most often a s aresult of leopard predati0n.3~Whetherthey moved as entire groups or as im-migrants into established groups, pre-dation increased when they spent timein unfamiliar areas. Immigrants weremost vulnerable during the first sixmonths after joining new groups.Thereafter, their vulnerability de-clined to a level comparable to that ofthe residents of the groups they hadjoined. This suggests that experiencedanimals did not pass on sufficientknowledge of the area to naive animalsto provide them with equal protectionfrom predators. Animals may be re-quired to learn this informationthrough their own experience.

Familiarity with an area may meanknowing the locations of shelters andthe patterns of individual predators,such as their favored ambush sites.The safest way for an animal to gainthis knowledge is to remain in thehome range where it was born. Many

The fact that even largerprimates, includingchimpanzees, aresubject to predationadds credence to thenotion that predationcould have been astrong selective forceon early hominids.

animals, including solitary ones, ap-parently follow this rule. They are spa-tially philopatric, remaining in theirhome ranges throughout their lives.40(This differs from the behavior of re-maining in one's natal group, whichmay or may not include spatial phi-lopatry.24) Predation may have favoredthe evolution of spatial philopatry; itmay also contribute to its mainte-nance. Spatial philopatry is consid-ered an important s tep in theevolution of group living because, in

many species, groups are composed ofrelated fema1es4O This is particularlytrue among Old World primates.Thus, once grouping became advanta-geous, predation may have contrib-uted to the evolution of kin-groups(pathway 3 in Fig. 1) .3) It appears that arboreal primatesare more vulnerable to predationwhen they are at forest edges, in openforest, o r on top of the canopy, wherethe sparseness of vegetation makesthem more visible and more accessi-ble than when they are in dense for-est.41-44 rimates that commonly usesuch areas-for example, black andwhite colobus (Cofobusguerezu)-may therefore be particularly vulner-able '+5,464) Predation, at least by mammals,may often be episodic. Condit andSmith reported that disappearancesof baboons at the Tana River Reserve,Kenya, which they attributed to lion(Panthera leo) predation, were epi-sodic.2yBusse observed leopardshunting roosting baboons in theMoremi Wildlife Reserve, Botswana,five times within a three-month pe-riod but only once in the 27 months ofobservation outside that time.3*Leop-ards were also implicated in an abruptincrease in disappearances of vervetsin Amboseli National Park, Kenya.During one 30-day period withm 526days of observation, 14 vervets disap-peared. This rate was more than seventimes greater than the rate during theprevious six months.32 One possible


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Predation Risk, Predation Rate, and the Effectiveness of Anti-predator TraitsOne measure of the effectiveness of anti-predator trailswould be the demonstration hat individuals, populations,orspecies that share a particular trait are subject to a lowerrate of predation than are individuals, populations,or spe-cies that do not exhibit this trait. However, of all the traits

listed in Table 1, the only ones that have been statisticallyrelated to variation in estimated predation rates are bodysize and group size (across species; see Fig. 2),5 humanpresence3* (Fig. 3a), and movement into unfamiliar areas 24or groups39 among groups within a population).Attempts tofind such direct patterns have failed for a number a traits,including group size32 intraspecific; Fig. 3b), terre~tr iality,~and birth synchrony.79These failures may sometimes, butnot always, be a result of the rarity of predation events.Partly in response to these failures, it has been recom-mended that we make a distinction between inherent pre-dation risk and realized predation rate.51For example, it ispossible that the failure to find that terrestrial primates ex-perience higher predation rates than do arboreal primatesmay be because terrestrial primates have evolved adapta-tions to deal with their inherently greater predation risk. Inthis context, presumedpredation risk may be an appropriatecorrelate of past selective pressure, whereas realized pre-

dation rate may be a better measure of present selectivepressure.Another use of the concept of risk is that it allows re-searchers to examine anti-predator traits even in popula-tions in which predation events are rarely documented. Forexample, the increased presence of predators or predatorsurrogates (models or humans), which is presumed to bean appropriate measure of predation risk, has been corre-lated with many of the traits in Table 1. This assumes, ofcourse, that researchers abilities to recognize risk are real-istic. This may not always be the case, as shown, for exam-ple, by the assertion that distance from trees is positivelyassociated with predation risk (see text).Vermeij7 has suggested that neither presumedpredationrisk nor realized predation rate is the best evolutionarymeasure of anti-predator adaptation. If all predation at-tempts are successful (or if all are unsuccessful), here canbe no selection or anti-predator traits, regardlessof the rateof predation. He suggests instead that the failure rate ofpredation attempts is the most appropriate measure. An ex-ample of this might be the difference in the abilities of pri-mate groups of different sizes to detect predators.l3


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68 EvolutionaryAnthropology ARTICLES

Polyspecific Associations: An Anti-predator Tactic?Mixed-species groups, inwhich troops of different primatespecies regularly feed and traveltogether, for hours, days, or evenweeks, are relatively commons1especially among guenons of Af-rica80-83 and small New World

monkey^.^^.^^ Such polyspecificassociations should entail in-creased feeding competition inspecies with significant dietaryoverlap or, at best, be neutral inspecies with little overlap. Mostecologists, herefore, have postu-lated enhanced predator aware-ness as he main benefit of suchassociations. Associating specieswould, in theory, reap severalbenefits, including increasedoverall awareness through thepresence of additional eyes andears; increased individual forag-ing time through decreased needfor vigilance per individual; andthe possibility that predators willconfront increased confusionwhen attacking a large group. Ob-servations that could be used totest the theory that polyspecific

Three guenon species from Gabon that frequentlyforage together in mixed-species groups: top, thecrowned guenon (Cercopifhecuspogonias):mid-dle, the spot-nosed guenon (C. nictitans): bottom,the moustached monkey (C. cephus). Thecrowned hawk eagle, a common predator onthese monkeys, soars overhead.associations are an effective anti predatory tactic, particularly for smaller spe-cies, have yielded interesting, but not definitive results. reported hatall 21 observed predation attempts by eagles on mixed-species groups onguenons in East Africa were unsuccessful, but could not demonstrate differ-ences in predators success rates in single-species groups versus mixedgroups. However, Gautier-Hion and colleaguesa2 eported hat three of the foursuccessful predation attempts by the eagles on Cercopithecus cephuswere onsingle-species groups, whereas only one attempt occurred when C. cephuswas foraging with other guenons (see Fig.). JG Fleagle

trial predators with extensive cover forambushes. Indeed, in the more openhabitats terrestrial primates may be atgreatest risk of predation nearest theirsleeping trees. The areas around thesetrees often provide cover for preda-tors, many of which hunt most ac-tively during the hours when primatesare either descending or ascendingtheir sleeping trees.

The assumption that the risk of pre-dation is greater for terrestrial pri-mates than arboreal primates isfurther weakened by evidence thatpredation on arboreal primates can besevere. There are terrestrial animals

that a re capable of killing arboreal primates, a t least in the Old World wherefossas (Ciyptoprocta fe~0~)30nd leop-ards occur. There are also avian preda-tors that specialize in killing arborealprimates in Africa, the Neotropics, thePhilippines, and M a d a g a ~ c a r . ~ ~ , ~ ~ , ~ ~ntwo studies of crowned eagles(Stephanoaetus coronatus) in KibaleForest, Uganda, monkeys accountedfor 87% and 89% of prey item^.^^,^^ InGuyana, monkeys, almost entirely ce-bids, were the most common prey ofharpy eagles ( H ap ri a h a p y j a ) , consti-tuting 36% of their diets.42The greymouse lemur (Microcebus mu r inu s )

represented 23% of the total biomasstaken by barn owls during one year inBeza Mahafdy, Madagasca~~On con-trast, no avian predators are known tospecialize in killing terrestrial primates.The vulnerability of arboreal pri-mates may also be increased by thefact that they generally are smallerthan terrestrial primates.34For exam-ple, small primates are prey for agreater number of avian predatorsthan are large primates. At least fivespecies of birds are confirmed or sus-pected predators of the 800 gm squir-rel monkey (Saimir i sciureus) in ManuNational Park, Peru, whereas only twospecies of birds are confirmed or sus-pected predators of the 3 kg capuchinmonkey in the same f o r e ~ t . ~ ~ , ~ *hevulnerability of small arboreal pri-mates is exacerbated by the fact thatsmall predators occur at greater den-sities than do large predators (see Ter-b0rgh,5~ p 194-195). On the otherhand, large body size may be seen asan evolutionary response to greaterpredation risk that has resulted inlower predation rates34 (see Box 3 ) .Nonetheless, these numerous lines ofevidence suggest that the actual inten-sity of predation on terrestrial pri-mates may have been exaggerated andthe intensity of predation on arborealprimates underestimated.

PRIMATES AS PRIMATEPREDATORSOnly a few studies of predation on

primates have been conducted on ha-bituated predators. Not surprisingly,those predators a re also primates.Chimpanzees (Pan troglodytes) , nottypically considered carnivores, nev-ertheless kill and eat animals, mostlyother primates. Primates accountedfor 62 to 100% of the observed verte-bra te prey of chimpanzees at threestudy sites in West and East Africa.5941Most of these (55 to 82%) were redcolobus (CoZobus badius ) . At GombeNational Park, Tanzania, at least 20%of the red colobus population was es-timated to have died in one year as aresult of chimpanzee predation.61Thesuccess of chimpanzees apparently in-creases with the number of males in-volved in hunting.

Stanford62 as examined predationby chimpanzees from the perspectiveof the prey. Groups of red colobus in


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Sex Roles inPredatorDefenseand VigilanceBased on observations that among savannah-dwellingprimates males are more aggressive than females in de-fense against predators, one early hypothesis of primate

social ecology suggested that such sex differences couldaccount for multi-male primate groups in predator-richhabi-t a t ~ . 5 0 ~ ~ ~ ~ ~ ~lternatively, multi-male groups may occur whenlarge female groups and close synchrony of female estrouscycles make it impossible for a single male to monopolizeaccess to breeding f e m a l e ~ 5 ~ ~ ~ ~bservations from manyspecies continue toshow that predator defense is often prin-cipally performed by males, even when there is only onemale in the group (see review by Cheney and Wrangham5).

Recently, several authors have suggested that a specialmale role against predators could account for monogamy interritorial marmosets,5l as well as multi-male group struc-tures in species with small female groups, such as capuchinmonkeys.72These recent twists on the original defense hy-pothesis are based on accumulating evidence that male pri-mates are significantly more vigilant than females.72 t hasbeen experimentally established that male capuchins, atleast, are more effective than females in detecting both aer-ial and ground predators. If females willingly mate with pe-ripheral subordinate males that are more likely to detectpredators, hese males will then have an incentive to remainin a group despite strong competition rom the dominant orresident male. CH Janson

the core areas of the chimpanzee com-munity home range averaged 46%smaller than groups at the periphery.Stanford attributed the smaller groupsizes to selective hunting of immaturered colobus and suggested that chim-panzee predation may limit redcolobus population size below cany-ing capacity. Expected changes in thebehavioral responses of red colobus inthe presence of chimpanzees did notalways occur. Groups became morecohesive and alarm calling occurredmore frequently as chimpanzees ap-proached, as expected. But eventhough the large group increased itsheight in the canopy when chimpan-zees were present, the smaller groupdid not. Stanford suggested that be-haviors such as early detection andflight, which are effective against am-bush predators, may not be as effec-tive against chimpanzees, which aresocial predators.Humans as Predators onPrimates

One major primate predator of pri-mates has thus far received little atten-tion as an agent of evolutionarychange in primates. Present-day hu-mans have been documented as majorpredators of primates in West andCentral Africa and in AmazonianSouth A m e r i ~ a . ~ ~ , ~ ~ndeed, in onestudy of mammalian predators inneotropical countries," human sub-sistence hunters killed more primatesin more sites than did either pumas(Felis concolor) or jaguars (Pantheraonca). Humans hunted primates in

three or four sites examined. In Ecua-dor, Venezuela, and Bolivia (same sitein different years), primates ac-counted for 20 to 66% of the preytaken by humans. In contrast, pumashunted primates in only one of foursites examined (Paraguay, 4% of preyitems) and jaguars in only one of threesites examined (Peru, 5% of preyitems). The greater presence of pri-mates in human diets may, in part, re-flect the greater ability of humans tohunt arboreal animals from a distancewith weapons. Indeed, another studysuggested that local Peruvian hunters

Figure 4. Mouse lemurs (Microcebus mufinus)have been reported to suffer extremely highpredation by the barn owl (Tyto alba) in south-western Madagascar. Figure by Luci Betti

have been so successful at killing pri-mates that the yields now appear to beunsu~tainable.6~

Human and nonhuman primateshave co-existed far longer in Africaand Asia than in the Neotropics andMadagascar. Although we do not yethave sufficient data to compare therates of human predation on OldWorld and New World primates, it ispossible that neotropical primateshave had less time to evolve adapta-tions to avoid predation by humansand, hence, are more vulnerable to ex-tinction as a result of hunting. Thismay have also been the case in Mada-gascar where, as recently as 2,000years ago, at least 15 species of pri-mates became extinct after the arrivalof humans, who not only hunted them,but also changed their habitats byburning and cutting forest, and intro-ducing domestic animals.66Differen-tial responses by Old and New Worldprimates to the threat posed by humanpredation have not yet been examined.This could be a fertile area for futurecollaborative research by cultural an-thropologists, primatologists, andconservation biologists.

CAN PREDATION REDUCEPRIMATE POPULATIONS BELOWCARRYING CAPACITY?It has been difficult to determine

whether predation or disease ever di-minishes animal populations belowthe levels that can be supported byavailable food.67Several catastrophicdie-offs of primate populations havebeen attributed to disease.68 but there


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is less evidence that predation has hadnegative effects on primate populationsize.A population of vervets may havebeen reduced below carrying capacityafter it suffered a sudden short-termincrease in predation.33 However,there had also been a consistent, long-term decline in its foodThe predation rate within one year ona population of grey mouse lemurs atBeza Mahafaly, Madagascar, has beenestimated at 25%,30 mong the highestfor any primate species (Fig. 4).s Be-cause its reproductive rates appear tobe high, however, this population maynot be limited by predati0n.3~f thereis any population that is limited bypredation, it might be found wherethere is little evidence of food compe-tition. For example, red colobus inKibale Forest, Uganda, show no obvi-ous behavioral expressions of foodcompetition, leading to the suggestionthat the size of this population may beconstrained, at least in the short term,by something other than food, such aspredation, disease, or social instabil-ity. It is noteworthy that the only pri-mate thus far thought to be limited bypredation is another population of redcolobus, in Gombe National Park,Tanzania.62

CONCLUSIONAlthough ecological patterns of pre-

dation on primates are now beginningto emerge, our confidence in thesepatterns depends on the intensity ofinquiry into the processes of preda-tion. If we are to understand theseprocesses, more studies of the interac-tions between predators and their pri-mate prey are greatly needed. Mostpromising, perhaps, ar e experimentalstudies in which the behavior of thepredator can be controlled. In thepast, such studies have included ob-servations of the responses of pri-mates to models of p r e d a to r ~ , ~ ~ , ~ 3ndto previously recorded alarm cal ls4Itwould be valuable to incorporatesimulated attacks into experimentalstudies. Another useful approachwould be for field biologists to organ-ize and conduct collaborative studiesin which the predators and the preyare habituated. Although habituationtakes time, the benefits of habituationfor observations of predator-prey in-teractions are unsurpassed. Until such

efforts are made, many of the out-standing questions in primate behav-ioral ecology will remain as hidden asa leopard in a bush,

ACKNOWLEDGMENTSI thank C. Janson and J . Fleagle for

inviting me to write this article. Manyof the thoughts presented here werestrengthened by discussions with T.Young, who contributed the materialin Boxes 1 and 2. J. Fleagle and C. Jan-son contributed the material in Boxes3 and 4. I am grateful to C. Stanfordand D . Overdorff for respondingpromptly to my requests for addi-tional literature, and to D. Cheney J.Fleagle, C. Janson, T. Young, and ananonymous reviewer for offering con-structive advice.

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