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atterns of injury in zoo-housed spider monkeys: A problem with males?

ick Davis a,b,*, Colleen M. Schaffner a, Stephanie Wehnelt b,c

Department of Psychology, University of Chester, Parkgate Road, Chester CH1 4BJ, UK

Chester Zoological Gardens, Upton-by-Chester, Chester CH2 1LH, UK

Am Klopferspitz 19, D-82152 Martinsried, Germany

Applied Animal Behaviour Science 116 (2009) 250–259

R T I C L E I N F O

rticle history:

ccepted 12 August 2008

vailable online 19 September 2008

eywords:

teles

uestionnaire

ale–male competition

ggression

oo

rimates

A B S T R A C T

Aggression among wild spider monkeys is most frequently reported to occur between the

sexes, with adult males directing aggression towards adult females and the aggression is

normally non-injurious. After two severe instances of aggression in the group of spider

monkeys housed at Chester Zoo, we developed a questionnaire to investigate the

frequency, direction and possible reasons for aggression in zoo-housed spider monkeys.

We sent our questionnaire to 55 zoos worldwide and obtained records from 26 groups,

which yielded detailed accounts of 143 aggressive incidents: 56 events for the actors and

127 events for the targets of aggression. We found that zoo-housed spider monkeys are

predominantly maintained in small social groups, with a single adult male, two adult

females and their offspring. Of the aggression reported, 23.1% of incidents resulted in

severe or lethal injuries. Adult males were the most frequent actors of aggression and

accounted for 66.7% of incidents. Six cases of male–male aggression were lethal. The most

striking pattern was that adult males directed aggression towards non-adult males more

than any other age/sex category. The most frequently reported context of aggression was

tension between adult and non-adult males. These findings contradict previous reports

from wild spider monkeys where female-directed male aggression is most frequently

reported. In light of our findings, we recommend that males form the core of the group and

that females be relocated among groups to reflect the wild condition of male philopatry

and female dispersal. In addition, enclosure design should allow opportunities for the

monkeys to segregate themselves from other group members, simulating fission, which is

a conflict management strategy for avoiding aggression in wild spider monkeys.

� 2008 Elsevier B.V. All rights reserved.

Contents lists available at ScienceDirect

Applied Animal Behaviour Science

journal homepage: www.elsev ier .com/ locate /applanim

1. Introduction

There is variation in the social organisation of non-human primates, ranging from solitary to pair living tomulti-male/multi-female communities, the latter com-monly characterised by female philopatry and maledispersal (Kappeler and van Schaik, 2002). In addition,most group-living species are characterised by a high

* Corresponding author at: Chester Zoological Gardens, Upton-by-

hester, Chester CH2 1LH, UK. Tel.: +44 1244 650 294;

ax: +44 1244 650 245.

E-mail address: n.davis@chesterzoo.org (N. Davis).

168-1591/$ – see front matter � 2008 Elsevier B.V. All rights reserved.

oi:10.1016/j.applanim.2008.08.008

degree of group cohesion. Some species (e.g., chimpan-zees, Pan spp. and spider monkeys, Ateles spp.) live ingroups that are characterised by a high degree of fission–fusion dynamics in which individuals travel in smallfluid subgroups or parties that change in membershipthroughout each day (Symington, 1990; Chapman et al.,1995). Fission–fusion dynamics are thought to haveevolved as a means to reduce intragroup competitionover spatially and temporally distributed fruit (Syming-ton, 1987, 1988, 1990; Chapman et al., 1989; Aureliet al., in press). In addition, fissioning is used as a way toreduce the escalation of aggression in wild spidermonkeys (Aureli and Schaffner, unpublished data). Asecond feature of chimpanzee and spider monkey social

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259 251

organisation is male philopatry and female dispersal, inwhich males remain in their natal group and femalesleave to join new groups upon reaching sexual maturity(Symington, 1990).

In the wild the spider monkeys average group rangesize is 278 ha (Di Fiore and Campbell, 2006), withcommunities varying in size from 15 to 56 individuals(Shimooka et al., 2008). The demographics of commu-nities are highly varied both across communities andspecies. There are reports of 1–15 adult males, 5–18adult females, 0–7 sub-adult males, 0–7 sub-adultfemales and 1–10 juveniles (Shimooka et al., 2008).Male–male social relationships are reported to be themost affiliative as they spend more time together andgroom each other more than any other adult age–sexcombination (Aureli and Schaffner, 2008). The reportedpattern of aggression in wild spider monkeys involvesmales targeting females most frequently. Males targetfemales by chasing them to the ground and very rarelyphysically attack females (Fedigan and Baxter, 1984;Symington, 1987; van Roosmalen and Klein, 1988;Campbell, 2003; Slater et al., in press). However,male–male aggression was unreported until recentlyin wild communities (van Roosmalen and Klein, 1988;Aureli and Schaffner, 2008), but two recent reportsindicate that male–male aggression can be severe and insome cases lethal among intra-community males(Campbell, 2006; Valero et al., 2006). Aggressionbetween females however appears to be rare in wildpopulations (van Roosmalen and Klein, 1988), althoughthere are reports of long-term resident females targetingnewer immigrant females (Asensio et al., 2008).

We observed two different incidents of male–maleaggression between the adult male and two juvenilemales at Chester Zoo. One case resulted in the death of ajuvenile male that was related to the adult male. As aconsequence, we realised very little information wasavailable about aggressive behaviour in zoo-housedspider monkeys. However, a variety of factors are knownto influence aggression in other captive primates, includ-ing the presence of human visitors in zoos, reduction intheir living space, changes in group composition, variationin reproductive and social status, and a lack of control overtheir physical and social environment (Honess and Marin,2005; Hosey, 2005; Morgan and Tromborg, 2007). There-fore, we developed a questionnaire to gather informationabout the direction, intensity and context of any reportedaggressive behaviour among zoo-housed spider monkeys.In addition, to investigate the influence of the physicalenvironment on the occurrence and pattern of theaggression, we requested information about enclosuredimensions. Based on the patterning of aggressionreported from field studies (see above), we made threesets of predictions. Firstly, adult males would be the mostfrequent actors of aggression and that adult femaleswould be the most frequent targets of minor aggression.Secondly, we predicted that adult males would be theactors of severe and lethal aggression and that the non-adult males would be the targets. Finally, we predictedthat females would be the least frequent actors ofaggression.

2. Methods

2.1. Procedure

We developed our questionnaire based on an earlier study that used a

similar tool for exploring patterns of aggression in captive lion tamarins

(Inglett et al., 1989; see Appendix A). Using the International Species

Information System (ISIS, 2004) we identified a total of 55 zoos world-

wide that maintained social groups of at least three adult spider monkeys

with a mixed sex composition. We distributed the questionnaire in

English in March 2002 and requested information on any recorded

aggressive events that had occurred in the previous 5 years

(Appendix A). In addition, we requested that any available animal record

keeping system (ARKS) or suitable zoo records which are maintained by

the keepers responsible for the spider monkeys, be returned with the

questionnaire. Our first question requested information about the species

of spider monkey. At the time of drafting the questionnaire four species

were housed regularly in zoos, including A. belzebuth, A. fusciceps, A.

geoffroyi and A. paniscus. However, A. fusciceps has recently been reclas-

sified and is now recognised as A. geoffroyi rufiventris (Rylands et al.,

2000). Our questions focused on the frequency, context, direction and

intensity of aggressive events; the age and sex of the individuals involved;

the group composition at the time of aggressive events and the patterning

of spider monkey aggression relative to other species that were housed at

the same zoo.

Adults included individuals older than 6 years of age and non-adults,

included individuals from 2 to 6 years of age (Symington, 1988). Infants

were not included in the analyses as they were not involved in any

aggressive interactions. The resulting age–sex categories were as follows:

adult males, adult females, non-adult males and non-adult females. The

aggressive incidents were classified into three categories of different

intensities based on the descriptions provided: ‘‘minor’’, which included

either no observed injuries or superficial injuries; ‘‘severe’’, which

included single or multiple wounds that required veterinary treatment;

and ‘‘lethal’’, when the individual was killed outright or where the injuries

were so serious they necessitated that the individual be euthanized.

Thirteen zoos provided information about the size of the spider monkey

enclosures. We requested the information following our main question-

naire as social behaviour, including aggressive interactions can be influ-

enced by the area of the enclosure (Kummer and Kurt, 1965; Judge and de

Waal, 1997; Caws and Aureli, 2003; Hosey, 2005) and the number of

individuals in the social group.

2.2. Analyses

Although information from 143 incidents was obtained, for the

investigation into actors and targets, only data where the identities of

either the targeted individuals (targets) or the actors of aggression

(actors) were known were analysed. This yielded 56 events for the actors

and 127 events for the targets of aggression. To ascertain whether the

distribution of the age/sex class of the actors or the targets of aggression

differed from a chance distribution we used x2-tests for goodness-of-fit.

The expected frequencies of aggression were weighted by correcting the

expected values by the proportion of individuals in each age/sex class in

the population to reflect the opportunity for aggression. To minimise the

potential for violating the underlying assumption of independence for x2-

tests, individual spider monkeys were counted only once for each cate-

gory of aggression. This had the effect of restricting our sample size, but

when sample sizes were less than six per cell we applied Yates correction

(Schwiegert, 1994). To assess whether there was a relationship between

the density of animals in the enclosure and aggression, we calculated the

density of 13 enclosures based on the modal number of animals in the

group over the course of the study and the area of the combined indoor

and outdoor enclosures. Pearson’s correlations were used to test for the

relationship between density and mean number of aggressive events. The

conventional alpha level of 0.05 was adopted for all tests.

3. Results

Thirty-two of the 55 questionnaires were returned(58%), although data from eight zoos (14.5%) had to beomitted because the group composition no longer met theminimum requirements for our study, or insufficient

Table 1

Composition of groups by species/subspecies for overall modal group size, modal number of adults and non-adults, modal number of males and females and

total number of aggressive incidents

Species/subspecies A. belzebuth A. fusciceps robustus A. geoffroyi A. paniscus Total

Number of groups 7 10 6 3 26

Modal group size 6 7 4 4 4

(adult/non-adult) (3/0) (6/0) (4/0) (2/1) (3/0)

(male/female) (1/2) (1/5) (1/3) (1/2) (1/2)

Total number of incidents 5 46 91 1 143

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259252

information was provided about the overall groupcomposition. Therefore, we had information regarding26 different groups of spider monkeys from 24 zoos. Therewere seven groups (26.9%) in which no aggression wasreported, which we subsequently refer to as non-aggres-sive groups, and 19 (73.1%) groups in which aggression wasreported, which we subsequently refer to as aggressivegroups. The modal overall composition for the data set(n = 26) was one adult male and two adult females. Themodal composition for non-aggressive groups (n = 7) wasone adult male and one adult female, while the modalcomposition for aggressive groups (n = 19) was one adultmale, two adult females and one non-adult male.

Four species were represented in the survey data A.

belzebuth (n = 7), A. paniscus (n = 3), A. geoffroyi (n = 6) andA. fusciceps (n = 10). A. fusciceps were kept in the largestoverall group sizes (including infants) and A. geoffroyi wereascribed the highest number of aggressive incidents(Table 1). However, x2 showed there was no significantdifference between the species designation for actors(x2(3) = 1.98; P > 0.05) or targets of aggression(x2(3) = 4.07; P > 0.05), therefore the entire data set,regardless of species, was pooled and analysed together.

3.1. Frequency of aggression

Using the criteria described above 127 cases ofaggression were recorded, with 93 cases (73.2%) of minoraggression, 28 cases (22.0%) of severe aggression and 6cases (4.7%) of lethal aggression reported. Half of therespondents considered the nature of spider monkeyaggression to be different to that of other primates housedwithin their zoos. Specifically, they reported aggressivebouts were less frequent, usually occurred without anyobvious signs of previous tension and often resulted in

Table 2

Summary of reported aggressive incidents towards adult male and non-adult m

Actors of aggression Targets of aggression

Adult male

Minor Severe Lethal

Adult male 1 3 1

Non-adult male 0 1 1

Adult female 1 0 0

Non-adult female 0 0 0

Group 9 2 0

Unknown 5 1 0

Total 16 7 2

more severe injuries to the target animals. They alsoreported that aggression often occurred when youngermales approached breeding age.

3.2. Actors and intensity of aggression

Overall, we found that males were much more likely tobe aggressors than females (x2(1) = 26.18; P < 0.001).When we examined the data further by age class, wefound that adult males were the most frequent actorsrepresenting 37 cases (66.1%), followed by non-adultmales who accounted for 11 cases (19.6%) and adultfemales who accounted for 8 cases (14.29%). There were noinstances of non-adult females as actors of aggression (seeTables 2 and 3). Analysis of all the intensities of aggressionrevealed an overall significant difference for actors(x2(3) = 28.25; P < 0.001). The finding was driven by theadult males who were more likely to be aggressors thannon-adult males (x2(1) = 18.01; P < 0.001), adult females(x2(1) = 19.09; P < 0.001) and non-adult females(x2(1) = 15.82; P < 0.001).

There was an overall difference in the distribution foractors of minor aggression from the expected distributionacross the four age/sex class categories (x2(3) = 14.85;P < 0.005). Age/sex pairwise comparisons yielded signifi-cant differences from the expected distribution as non-adult males were more likely to be the actors of minoraggression than adult males (x2(1) = 9.21; P < 0.005),adult females (x2(1) = 8.19; P < 0.005) and non-adultfemales (x2(1) = 7.88; P < 0.005). When we examinedthe distribution of severe aggression we found that therewas also a difference in the distribution for actors acrossthe four age/sex classes than expected (x2(3) = 9.38;P < 0.025). The significant difference from the expecteddistribution was driven by the adult males as they were

ale spider monkeys as classified by age, sex and intensity

Non-adult male

Total Minor Severe Lethal Total

5 8 3 2 13

2 1 0 1 2

1 3 0 0 3

0 0 0 0 0

11 2 1 0 3

6 13 7 1 21

25 27 11 4 42

Table 3

Summary of reported aggressive incidents towards adult female and non-adult female spider monkeys as classified by age, sex and intensity

Actors of aggression Targets of aggression

Adult female Non-adult female

Minor Severe Lethal Total Minor Severe Lethal Total

Adult male 11 2 0 13 5 1 0 6

Non-adult male 6 0 0 6 1 0 0 1

Adult female 3 1 0 4 0 0 0 0

Non-adult female 0 0 0 0 0 0 0 0

Group 6 1 0 7 2 1 0 3

Unknown 15 1 0 16 1 3 0 4

Total 41 5 0 46 9 5 0 14

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259 253

more likely than expected to target severe aggressioncompared to non-adult males (x2(1) = 5.56; P < 0.025),adult females (x2(1) = 7.16; P < 0.01) and non-adultfemales (x2(1) = 7.33; P < 0.01). Finally, the distributionfor actors of lethal aggression differed from an expecteddistribution across the four age/sex classes (x2(3) = 11.38;P < 0.01). The difference was due to adult males beingmore likely than expected to be responsible for lethalaggression compared to non-adult males (x2(1) = 5.03;P < 0.025), adult females (x2(1) = 8.48; P < 0.005) andnon-adult females (x2(1) = 7.10; P < 0.01).

3.3. Targets and intensity of aggression

Overall, males were more likely than expected to bethe targets of aggression, regardless of intensity (x2(1) =18.29; P < 0.001). Adult females were the targets ofaggression in 46 cases (36.2%) of the aggressive boutsreported. Non-adult males were the targets of aggressionin 42 of the cases (33.1%), adult males in 25 cases (19.7%)and non-adult females were targets of aggression in 14 ofthe cases (11.0%) (Tables 2 and 3). The distribution acrossage/sex categories for all aggression differed from theexpected distribution (x2(3) = 51.37; P < 0.001); however,the significant effect was attributable to non-adult maleswho were more likely to be targeted than expectedcompared to adult males (x2(1) = 42.69; P < 0.001), adultfemales (x2(1) = 50.94; P < 0.001) and non-adult females(x2(1) = 43.07; P < 0.001).

When we examined the distribution according to thedifferent intensities more variation in the pattern wasidentified. The distribution across age/sex categories forminor aggression differed from the expected distribution(x2(3) = 26.02; P < 0.001). The deviation from theexpected distribution was due to non-adult males receiv-ing more minor aggression than expected compared toadult males (x2(1) = 20.92; P < 0.001), adult females(x2(1) = 23.71; P < 0.001) and non-adult females(x2(1) = 21.87; P < 0.001). The distribution for targets ofsevere aggression also differed from the expected dis-tribution across the four age/sex classes of individuals(x2(3) = 13.14; P < 0.005). The deviation also differed dueto non-adult males receiving more severe aggression thanexpected compared to adult males (x2(1) = 10.50;P < 0.005), adult females (x2(1) = 12.63; P < 0.001) andnon-adult females (x2(1) = 10.22; P < 0.005). Finally, thedistribution for targets of lethal aggression also differed

from expected (x2(3) = 25.17; P < 0.001). Non-adult maleswere more likely than expected to be targets of lethalaggression than adult males (x2(1) = 18.56; P < 0.001),adult females (x2(1) = 22.84; P < 0.001) and non-adultfemales (x2(1) = 20.23; P < 0.001).

3.4. Animal density

We found no correlation between the density of spidermonkeys and total mean number of aggressive events(r = 0.08, P = 0.81). Furthermore, no significant correlationswere found between density and mean number of minoraggressive events (r = 0.08, P = 0.79), severe aggressiveevents (r = 0.03, P = 0.93) and lethal aggressive events(r = �0.13, P = 0.67).

3.5. Context of aggression

Of the 143 cases of aggression a detailed explanationwas provided by the respondents for 54 (37.8%) of theincidents, and these were separated into five distinctcontexts. The most frequent context for aggression wastension among males within the same group, which wasreported by 10 zoos and accounted for 50% of the incidentsdescribed. The context of introduction, when animals werereintroduced to the group after a period of separation orwhen new animals were introduced to the group, wasreported by seven zoos accounting for 25.9% of theincidents. ‘‘Bullying’’ when the whole group chased andharassed an individual was reported in four zoos account-ing for 20.4% of the incidents described by zoo keepers. Theleast frequent context of aggression was public feedingreported by one zoo accounting for 3.7% of the incidents.General aggression in the group, aggression by males andaggression by females were also reported, but not enoughdetail was provided to indicate a specific context.

4. Discussion

The questionnaire provided information about 143aggressive incidents which we used to evaluate ourpredictions. The first prediction was that adult maleswould be the most frequent actors of minor aggression andthat adult females would be the most frequent targets ofminor aggression. Although adult males were responsiblefor the majority of the reported minor aggression, with 25of the 40 individual cases, and adult females received 41 of

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259254

the 93 cases of minor aggression, when their populationproportions were taken into account the results did notsupport either of these predictions. It was the non-adultmales who were more frequently the actors and the targetsof minor aggression than expected. This differs fromreports in the wild, which indicate female-directed maleaggression is the most frequently reported aggression(Fedigan and Baxter, 1984; Campbell, 2003; Slater et al., inpress). Reports of minor aggression between males arevirtually absent from wild populations. For example, vanRoosmalen and Klein’s (1988) review does not include anyreports of male–male aggression.

The second prediction, that adult males would be themost frequent actors of severe and lethal aggression andthat the non-adult males would be the most frequenttargets was supported. Adult males were overwhelminglyresponsible for severe and lethal aggression. Malescommitted nine of the 11 cases of severe aggression. Inaddition, non-adult males were more likely than expectedto be the targets of severe and lethal aggression. Theproportion of aggressive incidents that resulted in severeinjuries (22.0%) is high compared to data from severallong-term studies of captive primates in which no severeaggression was reported (Bernstein et al., 1983; Thierry,1985; Ren et al., 1991; Zucker, 1994; Fuentes et al., 2002).Males were responsible for all five to six cases of lethalaggression. Incidents of lethal aggression in captivity arealso rare and previously have been reported only in captivechimpanzees (de Waal, 1986) and golden lion tamarins(Inglett et al., 1989). However, there are more reports oflethal aggression in wild primates. Itani’s (1982) reviewrevealed killing occurred in 13 species from nine genera ofprimates. Recent studies reveal that lethal intragroupaggression also occurs in gibbons (Palombit, 1993),chimpanzees (Nishida, 1996; Fawcett and Muhumuza,2000; Watts, 2004; Watts et al., 2006), capuchin monkeys(Gros-Louis et al., 2003) and spider monkeys (Campbell,2006; Valero et al., 2006).

Finally, we predicted that females would be the leastfrequent actors of aggression. Our data supported thisprediction as only eight incidents of aggression wereattributable to adult females, and all but one incident wascategorised as minor. Non-adult females were never theactors of aggression. This is not surprising as very low ratesof female–female aggression are reported in wild popula-tions of spider monkeys (Fedigan and Baxter, 1984; vanRoosmalen and Klein, 1988), with the exception thatresident females do target aggression towards newimmigrant females (Asensio et al., 2008). However, theanalogous context, the introduction of a new female intoan existing group, only occurred one time in our studygroups and did not result in any female–female aggression.

One explanation for the pattern of aggression weidentified is that male–male aggression in zoo-housedspider monkeys may reflect natural behaviour that occursin wild communities. Intragroup aggression betweenmales has been reported in the wild and recent studiesfrom two field sites (Campbell, 2006; Valero et al., 2006)indicate that male–male aggression, albeit rarely observed,may be more serious than the more commonly reportedmale–female aggression (Fedigan and Baxter, 1984; van

Roosmalen and Klein, 1988). Valero et al. (2006) reportedon a single lethal attack, while Campbell (2006) reportedon three separate attacks, which all resulted in seriousinjuries and in two cases had a presumed lethal result. AtCampbell’s field site, all three attacks involved a coalitionof resident adult males attacking a single non-adultresident male. Such intragroup lethal aggression issurprising given that males are philopatric, are likely tobe related and have the strongest social bonds. Forexample, males affiliate with each other more frequently(Ahumada, 1992) and travel in all male subgroups morethan other age/sex classes (Shimooka, 2005). In addition,males defend their territory during intergroup encounters(Klein, 1974; Symington, 1990), and make joint raids intoneighbouring communities (Aureli et al., 2006). There isalso negligible sexual dimorphism in spider monkeys,which has been linked to low levels of male–malecompetition (Fedigan and Baxter, 1984; Dixson, 1998).

Further support for the finding that males areresponsible for the majority of aggression in zoos wasprovided by questionnaire respondents. Zoo keepersindicated that the most frequent context of aggressionwas ‘‘tension’’ between males. These descriptions indi-cated that this context represented a long-standingsituation between two males in which they had repeatedconflicts that were not resolved. In addition, this tensionwas particularly noted to occur between non-adult andadult males. The remaining contexts of aggression, feedingby zoo visitors and reintroducing group members orintroducing new group members are well-establishedsources of short-lived aggression in a variety of primatetaxa (Honess and Marin, 2005; Hosey, 2005). There wasalso a consensus by the respondents that aggression inspider monkeys differs to that of other primate species. Inparticular, spider monkey aggression was characterised asinfrequent, involving non-adult males more often and wasmore severe than what the keepers observed in otherprimate species.

Several explanations might account for the higher thanexpected levels of aggression between males reported inzoos. Firstly, one proximate mechanism in promotingbetter relationships among males is the need to cooperatein defending their home territory (Aureli et al., 2006). In azoo setting, the absence of rivals may reduce the value ofmale social relationships (Aureli et al., 2002) and lead to agreater degree of male intolerance. A second explanationmay lie in the management practices of zoos. Males areregularly relocated between zoo groups (Pierre Gay,personal communication), which does not correspond tothe pattern of immigration in wild groups where femalesdisperse (Klein and Klein, 1971; Fedigan and Baxter, 1984;Symington, 1990; van Roosmalen and Klein, 1988;Ahumada, 1992). Such practices inevitably lead to moreunrelated males housed together than would occur in thewild, which could be further a source of tension (seeEisenberg and Kuehn, 1966). The practice of relocatingmales and not females (Durlot and Gay, 1998; Newland,1999) could influence rate and intensity of aggression,although this factor was not explicitly examined in thequestionnaire. While there may be management difficul-ties keeping groups of spider monkeys in their ‘‘natural’’

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259 255

group structure its feasibility should be investigated,particularly as maintaining animals in abnormal socialgroupings is a known source of stress (Honess and Marin,2005; Hosey, 2005; Morgan and Tromborg, 2007). A policythat would include the transfer of females, and not males,between zoos would not be unprecedented as this is thegeneral management policy for chimpanzees in zoos (Fulk,2000; Carlson, 2006).

Finally, it is well established that captive environmentsmay alter the behaviour of individuals relative to their wildcounterparts (Kummer and Kurt, 1965; Hosey, 2005).Specifically, Hosey (2005) highlighted that for zoo-housedprimates the presence of visitors, restricted space andmanagement practices all impact behaviour, and socialfactors are likely to interact with these variables. Forexample, the social system of a given species, which canvary in the extent of group cohesion and mating patterns(van Schaik and van Hooff, 1983), could be influencedunder captive conditions. Therefore, individuals that live insocial systems characterised by a high degree of fission–fusion dynamics could be particularly affected given thatin the wild they have the option of leaving a subgroup toreduce conflict (Aureli and Schaffner, 2007). Althoughwe did not find a positive relationship between thedensity of the spider monkeys in zoos and the number ofaggressive episodes this could be explained by the copingstrategies adopted by other primates when restricted to aconfined space (Aureli and de Waal, 1997; Judge and deWaal, 1997; Caws and Aureli, 2003). However, smallenclosures do reduce opportunities for fissioning, whichmay influence the intensity of aggression in zoo-housedspider monkeys.

5. Conclusion

Collectively, the lack of rival males, housing unrelatedand unfamiliar males together and having no means to

simulate fission are factors that may lead to patterns ofmale aggression that exceed what would be expected bychance alone. These factors also indicate the importance ofproviding suitable housing and husbandry practices forspider monkeys. Specifically, larger and more complexenclosures that allow opportunities for individuals totemporarily separate themselves from the larger socialgroup, in order to simulate fission events in the wild, mayreduce the frequency and severity of aggression (Cawset al., 2008; Wehnelt et al., 2006). The unnatural social andphysical environment in which spider monkeys tend to bekept in zoos may exacerbate the propensity for male–maleaggression in the wild. Therefore, managing zoo popula-tions of spider monkeys should entail relocating femalesrather than males. Finally, our results highlight apreviously little known phenomenon.

Acknowledgements

We thank Pierre Gay, the European Studbook Keeperfor assistance and support in distributing the question-naire. In addition, we thank the many zoo keepers,curators and research personnel at the following zoosthat made our study possible: Aalborg Zoo, ApenheulPrimate Park, Artis Zoo, Auckland Zoological Park, TheBaltimore Zoo, Banham Zoo, Barcelona Zoo, ZoologischerGarten Berlin, Bristol Zoo Gardens, Cleveland MetroparksZoo, Colchester Zoo, Copenhagen Zoo, Noorder DierenparkZoo Emmen, Frankfurt Zoo, John Ball Zoo, Zoo Koln, ZooLandau in der Pfalz, Zoological Society of London, Zoo deMullhouse, Zoo Osnabruck, Omaha’s Henry Doorly Zoo,Peaugres Zoo, Rotterdam Zoo, Santa Ana Zoo, Sequoia ParkZoo, Zoological Society of San Diego, Staten Island Zoo,Suffolk Wildlife Park, Twycross Zoo, Wilhelma Zoolo-gisch-Botanischer Garten, Zoo Wuppertal, and in parti-cular Chester Zoological Gardens and ISIS. We are alsograteful to Filippo Aureli and Vicky Melfi for comments.

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259256

Appendix A. Spider monkey survey

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259 257

N. Davis et al. / Applied Animal Behaviour Science 116 (2009) 250–259258

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