Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defence and assessment of neighbours

ANIMAL BEHAVIOUR, 2001, 62, 11–21 doi:10.1006/anbe.2000.1726, available online at http://www.idealibrary.com on

Intergroup interactions in wild common marmosets, Callithrix jacchus: territorial defence and assessment of neighbours CRISTINA LAZARO-PEREA

Department of Zoology, University of Wisconsin-Madison (Received 22 March 2000; initial acceptance 4 June 2000; final acceptance 4 December 2000; MS. number: A8755)

Group territoriality associated with aggressive intergroup interactions is characteristic of most cooperatively breeding species. Neighbours, however, are not only competitors but also potential mates. Intergroup interactions might provide a direct mechanism for the assessment of breeding opportunities in neighbouring groups. I studied 228 intergroup interactions in wild cooperatively breeding common marmosets to understand how animals might balance their cooperation in territorial defence with their assessment of neighbours as potential mates. Intergroup interactions included both agonistic and nonagonistic behaviour. Aggression was directed primarily to same-sex individuals. Reproductive females’ involvement in intergroup interactions decreased during the last 2 months of pregnancy and during the first 2 months of lactation. Subordinate females participated more often than reproductive females in territorial defence but they were also more involved in nonagonistic interactions with animals from other groups. Intergroup copulations involved mainly subordinate females, and occurred both during forays into other groups and during agonistic intergroup encounters in the subordinate female’s territory. Eldest helper females were more likely than younger females to chase away other individuals, but were also more likely to engage in extragroup copulations. Cooperation by helpers in territorial defence might decrease the cost of defence for the breeders. Furthermore, our data indicate that assessment of neighbours does not occur solely during individual forays into other groups’ territories. Helpers’ participation in intergroup interactions in their own territory might provide direct benefits related to dispersal decisions as well by allowing nonreproductive individuals to assess individuals from neighbouring groups, evaluate potential breeding vacancies and increase familiarity with neighbouring groups. 

mystax, Garber et al. 1993; common marmosets, Hubrecht 1985). Many cooperatively breeding systems are also characterized by a despotic partition of reproduction that might affect the involvement of breeders and helpers in intergroup interactions. In order to breed, helpers must either wait to inherit a reproductive position in their natal group (which typically involves the immigration of an opposite-sex animal from a neighbouring group), or disperse and attempt breeding elsewhere, most commonly in a neighbouring territory (e.g. superb fairy-wrens, Malurus cyaneus, Pruett-Jones & Lewis 1990; dwarf mongooses Keane et al. 1996; suricates, Suricata suricatta, Doolan & MacDonald 1996; golden lion tamarins, Baker et al. 1993; saddle-back tamarins, Saguinus fuscicollis, Goldizen & Terborgh 1989). Which option is chosen probably depends on changing demographic and environmental conditions that determine the availability of territories or mates in the population. If correct assessment of breeding opportunities both in their own and in neighbouring

Cooperatively breeding species, in which nonparental adults regularly aid in the rearing of young (Emlen 1991), typically defend all-purpose territories against neighbouring groups and intruders (Gaston 1978). Cooperation in territorial defence is frequently cited as one way in which helpers collaborate with the breeding pair while remaining in their natal group (e.g. Cockburn 1998). Intergroup interactions in these species are frequently described with terms that emphasize their aggressive component such as ‘territorial fights’, ‘aggressive intergroup encounters’, or ‘boundary conflicts’, and have been documented in wild populations of cooperatively breeding fish (reviewed in Taborsky 1994), birds (see studies in Stacey & Koenig 1990), and mammals (silverback and golden jackals, Canis mesomelas and C. aureus, Moehlman 1986; dwarf and banded mongooses, Helogale parvula and Mungos mungo, Rood 1986; golden lion tamarins, Leontopithecus rosalia, Peres 1989; moustached tamarins, Saguinus Correspondence: C. Lazaro-Perea, Triana 47, Madrid 28016, Spain (email: [email protected]). 0003–3472/01/070011+11 $35.00/0

2001 The Association for the Study of Animal Behaviour

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2001 The Association for the Study of Animal Behaviour

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ANIMAL BEHAVIOUR, 62, 1

groups is a critical component of reproductive success of helpers, then helpers should evaluate their options frequently (Emlen 1997). Forays into other groups are believed to be the main mechanism by which animals obtain information and increase familiarity with neighbouring territories and groups. Such ‘stay-and-foray’ strategies (Brown 1987) are known to occur in a diversity of species (e.g. Florida scrub-jay, Aphelocoma coerulescens, Woolfenden & Fitzpatrick 1990; white-winged trumpeters, Psophia leucoptera, Sherman 1995; acorn woodpeckers, Melanerpes formicivorus, Mumme & de Queiroz 1985; suricates, Doolan & MacDonald 1996). Territorial defence and assessment of neighbours have been generally addressed separately in the literature. However, residents do not necessarily need to leave their territories to gain information about neighbouring groups. During intergroup and intruder encounters individuals from neighbouring groups come into proximity with the residents. Thus, aggressive interactions in the natal territory also provide an opportunity for breeders and helpers to gather information and assess neighbouring individuals and groups. Consequently, helpers’ involvement in intergroup interactions can have implications for both within-group cooperation and dispersal decisions, which remain two of the most important issues in the study of cooperative breeding (Solomon & French 1997; Heinsohn & Legge 1999). In this paper, I examine the factors that influence the participation of different group members in intergroup and intruder encounters in relation to both territorial defence and assessment of neighbours in a wild population of a territorial and cooperatively breeding primate, the common marmoset. Common marmosets live in small groups of 3–15 individuals in a variety of habitats in northeastern Brazil (Stevenson & Rylands 1988). Typically, only one female reproduces within the group (but see Digby & Ferrari 1994). Male and female offspring of the breeding pair remain in their natal group past puberty, and both sexes might disperse (Araujo 1996; Monteiro da Cruz 1998). Home ranges are small (<1 to 8 ha), have variable areas of overlap with neighbouring home ranges, and are defended against other groups and single intruders (Hubrecht 1985; Stevenson & Rylands 1988). Intergroup encounters are frequent in wild populations (1.9 encounters per observation day, Hubrecht 1985) and both aggressive and nonaggressive behavioural interactions (including intergroup copulations) have been observed during those encounters (Hubrecht 1985; Digby 1999). In captivity, common marmosets’ reactions against strangers are affected by sex of resident and intruder (Epple 1970; Harrison & Tardif 1989), presence of mate or rest of family (Anzenberger 1985; Harrison & Tardif 1989), social status within the group (Epple 1970; Anzenberger 1985), whereas black tufted-ear marmosets’, C. kuhli, reactions are affected by group size (Schaffner & French 1997) and familiarity with intruders (French et al. 1995). In addition, captive breeding female marmosets decrease the time spent locomoting during the last 2 months of pregnancy, increase their foraging time and energy intake and decrease the time spent in active social interactions during lactation (Price 1992; Nievergelt &

Martin 1999). Similarly, alloparental care can impose great energetic burdens on helpers, which might lose up to 11% of their body weight even in captive conditions, in other cooperatively breeding species (wild suricates, Suricatta suricata, Clutton-Brock et al. 1998; captive cottontop tamarins, Saguinus oedipus, Sa´ nchez et al. 1999). Therefore, participation in intergroup interactions by different group members might be affected by the constraints imposed by reproduction and the presence of infants in the group. One additional factor to consider is the position of helpers in the reproductive queue: younger daughter captive common marmosets do not ovulate when an older sister is present in the family (Saltzman et al. 1997), and dispersal seems to be more common among older females in the wild (Araujo 1996; Monteiro da Cruz 1998). Previously we reported changes in inter- and intragroup relationships between male and female common marmosets when reproductive vacancies appeared in several wild groups (Lazaro-Perea et al. 2000). After breeding positions became available, extragroup copulations between residents and future immigrants became more frequent during intergroup encounters and allowed subordinate females to have access to mates and to become pregnant (presumably due to extragroup copulations, based on behavioural data) before demographic changes took place. Intragroup conflict between males and females during intergroup interactions suggested that the encounters were being used to pursue different interests by males and females: males attacked females from their own group after those females had chased extragroup females away or spent time in proximity with extragroup males. This evidence is consistent with the hypothesis that involvement in intergroup interactions in the home range can be related not only to territorial defence, but also to the assessment of neighbouring animals. Here I explore this hypothesis further by evaluating how group composition, sex of the intruders, reproductive condition of the breeding female and relative age of the helpers influence individual participation in aggressive and nonaggressive intergroup interactions during periods of group stability. If intergroup interactions in the natal territory are not only used for territorial defence but also for assessing breeding opportunities in neighbouring groups, then the involvement of different individuals should reflect their trade-off between cooperation in territorial defence and their interest in neighbours as potential mates. Specifically, breeding animals should be involved in aggressive interactions against neighbouring groups and intruders, mainly against same-sex animals, whereas nonreproductive individuals should be involved in both aggressive and nonaggressive interactions with neighbours. In addition, if energetic and mechanical constraints associated with reproduction affect participation in intergroup interactions, we expect that the participation of the breeding female would decrease during the last part of pregnancy and lactation. Participation by helpers should also decrease during the period of infant dependence either in all helpers, or in the helper carrying the infants at the time of the intergroup interaction. Finally, if eldest

LAZARO-PEREA: INTERGROUP INTERACTIONS IN MARMOSETS

Table 1. Study groups: data set for description of behavioral patterns observed during intergroup interactions

Group

Group size

Habitat†

Observation period

P PF* PM* Q E E2* M PB PBF* PBM*

5–6 2–3 4–5 9–10 6–7 5–6 5 7–10 5–7 5

P P P P F F F F/C C C

Sept 1996–July 1997 July 1997–Sept 1997 July 1997–Nov 1997 Sept 1996–Nov 1997 Sept 1996–May 1997 May 1997–Nov 1997 Nov 1996–Apr 1997 Dec 1996–Sep 1997 Sep 1997–Dec 1997 Sep 1997–Dec 1997

Observation hours

Total number of intergroup interactions

283 38 87 391 233 154 97 274 97 75

103 6 3 104 30 19 21 42 9 2

*Groups PF, PM, PBF, PBM and E2 were not completely independent of groups P, PB and E, but were considered different social units due to substantial changes in composition and shifts in home range area. Groups PF and PM resulted from the fission of group P in July 1997, and groups PBF and PBM resulted from the fission of group PB in September 1997. In group E, the breeding female, nonreproductive female and a 5-month-old infant disappeared in May 1997, and a new adult female immigrated into the group and became the breeding female; from that point this social unit was considered a different group (E2). †Habitats: P=Plantation; C=Coconut plantation outside EFLEX-IBAMA; F=Forest.

adult helpers are more likely to emigrate and to inherit the reproductive position at the natal home, they should be more involved than younger same-sex helpers in both aggressive interactions against same-sex neighbours and nonaggressive interactions with opposite-sex neighbours. METHODS

Study Population This study was conducted at the Nisia Floresta Forest Experimental Station, EFLEX-IBAMA (Brazil). The research station (65 S, 3512 W) is located about 40 km from Natal, the capital of the state of Rio Grande do Norte, northeastern Brazil. This station covers 70 ha of secondary Atlantic forest, 50 ha of Tabuleiro vegetation, and 50 ha of experimental plantation (exotic trees, mainly Eucalyptus citridora) and is surrounded by coconut plantations (Santee & Arruda 1994). The study groups inhabited all those habitats (Table 1). Data were collected between September 1996 and December 1997. We began observing five social groups, three of which experienced substantial demographic changes (including the fission of two of the groups, Lazaro-Perea et al. 2000) and shifts in home range area during the course of the study. The resulting groups were considered different social units after those changes, resulting in a total of 10 different social units being observed (Table 1; for a similar criterion see Dietz et al. 1997). All animals (except one adult female from group PB and one adult male of group E) were fitted with coloured bead collars and/or dyed with picric acid in different body areas to allow for individual identification. Males of three different groups (one male in each) were fitted with a radio transmitter (Telonics, Inc., Mesa, Arizona, U.S.A.) to facilitate the location and following of the groups (see Savage et al. 1993 for a similar method in wild cottontop tamarins).

Data Collection All-day or half-day follows were carried out by the author and two trained observers for each group in rotation, so that each group was observed usually at least one day every week (Table 1). Ten minute focal animal samples were carried out for all animals older than 12 months of age in each group. Whenever one or more animals from the focal group were seen approaching animals from another group, or when one or more extragroup animals were detected in the focal group territory, we stopped all other data collection and started collecting data on the intergroup interactions. Behavioural data were dictated into a tape recorder and included the date, time, location, groups involved, animals involved and description of behavioural patterns observed during the interactions (Table 2). Only those encounters in which we could identify individually the participants from at least one of the groups were included in the analyses. Vocalizations heard during intergroup interactions were also recorded and I classified them into seven different categories (Table 2). Exchanges of vocalizations between animals of two different groups were included in the analyses only when they were accompanied by some other behavioural interaction. Two consecutive interactions among animals of two given groups were considered two separate intergroup interactions when there was more than 30 min between them. One animal was considered to participate in an encounter when it was seen vocalizing or performing any behavioural pattern directed to an animal from the other group (e.g. resting in the proximity of the encounter site during the encounter did not qualify as participation). When animals from the focal groups interacted with animals from unmarked groups, we attempted to determine the size of the unmarked group and the sex of as many individuals as possible.

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ANIMAL BEHAVIOUR, 62, 1

Table 2. Behaviours recorded during intergroup interactions Percentage of interactions Intergroup (N=168)

Behaviour

Definition

Long calls*

Loud, long vocalizations with a mostly horizontal shape (phee calls in Epple 1968) Series of short, ascending calls (twitter in Epple 1968) Brief, descending calls with broad frequency range. Given singly and in series (mobbing calls in Epple 1968) Low-pitched, staccato chattering (Epple 1968) String of vocalizations that included nga-nga (low-pitched, atonal, infantile squeals Epple 1968) Brief, high-pitched vocalizations (warning calls in Epple 1968) Any vocalization that could not be classified in any of the previous categories Climb on partner’s back from behind and grip partner around waist and legs, with genitals in close proximity to partner’s genitals or tail Move (not running) towards an animal from another group without displaying any sign of aggression Raise tail to expose genitals to partner Pelage erected. Usually animal presented arched back Rub anogenital area against substrate Put anogenital area on top of groupmate Jerk the body towards partner or pursue partner aggressively, without contact aggression Grab, hit, or bite partner

Stacattos* Tsiks* Ehr-ehr* Submissive vocalizations* Alarm calls* Other vocalizations* Copulation or attempted copulation

Nonaggressive approach Genital display Piloerection Scent marking Marking partner Chase+lunges Contact aggression

Intruder (N=60)

81.4

60

72.6 74.2

35.6 31.1

41.9 56.4

15.6 46.7

19.3 14.5

2.2 2.2

11.9

20

12.5

35

79.8 45.2 47.6 5.9 79.2

38.3 31.7 28.3 1.7 61.7

25.6

8.3

*Vocalizations were only recorded by one of the observers and therefore percentages are calculated for a subset of interactions (Nintergroup encounters =124, Nintruder encounters =45).

Data Analyses For description of behavioural patterns and vocalizations observed during intergroup interactions, I used data from the 10 different social groups during the entire study period (Table 1). For analyses of participation in intergroup interactions depending on social/reproductive status, I used data only from (1) stable periods in which groups had both reproductive and nonreproductive females and (2) those six groups that were observed a minimum of 6 months and had participated in a minimum of 15 intergroup interactions (Table 3). I classified animals in each group into four broad age categories at the beginning of observations: infant (0–5 months old), juvenile (6–10 months old), subadult (11–15 months old), and adult (>15 months old) following Stevenson & Rylands (1988). The age classifications are meant to indicate relative ages only. For some individuals the approximate date of birth was available, but for most animals, I estimated age using body size (weight measures taken during capture, see Araugo et al. 2000 for weights of the different age classes) and morphological characteristics such as coloration of ear tuffs (juveniles already presenting all-white tuffs), and dental development. For the classification of adults between breeding and nonbreeding, I used the evidence of pregnancy and lactation of infants for females (within each group, the female that was observed to be pregnant and subsequently nursing infants was classified as reproductive/ dominant female), and grooming relationships with the

breeding female for males. In all groups with more than one adult male (N=4), the male that showed a greater affiliative relationship with the reproductive female could be determined unambiguously by his affiliative relationship with the breeding female (he spent at least 50% more time grooming with the reproductive female than the other male(s) of the group) and was classified as the Table 3. Study groups: data set for study of individual participation in intergroup interactions

Group

P* Q E* E2 M PB*

Total number of intergroup interactions

36 104 29 19 21 20

Group composition†

F, F, F, F, F, F,

M, M, M, M, M, M,

2f, 2m m, 5f, 2sbf, 2 in m, 2f, 1sbf, 1jvm, 1jvf f, m f, 2sbf, 2 in 4f, 2sbf, jvf, jvm, in

*Groups P, E and PB lost their reproductive female in December 1996, April 1997 and May 1997, respectively. Only intergroup interactions that occurred prior to the death of the reproductive females were used for analyses of participation by different group members. †F=Breeding female; M=putative breeding male; f=subordinate/ nonreproductive adult female; m=subordinate/nonreproductive adult male; sbf=subadult female; sbm=subadult male; jvf=juvenile female; jvm=juvenile male; in=infant. See text for explanation of the different categories.

LAZARO-PEREA: INTERGROUP INTERACTIONS IN MARMOSETS

putative reproductive/dominant male. The grooming data agreed with observations of mate-guarding behaviour of these males during the postpartum oestrus of the females in three of the groups. Genetic data from the same population indicated that behaviourally dominant males that had strong social bonds with the dominant female could not be excluded as fathers for 10 of 11 infants born in the three groups studied (Nievergelt et al. 2000). In group E2, there was a change in the affiliative relationships of the two males with the breeding female after the birth of infants and both males were seen copulating with the female during her postpartum oestrus. Analyses were repeated considering each of these males as the putative breeding male, but results did not vary. The classification of males and females in dominant and subordinate categories using the above criteria was supported by agonistic data from all dyads for which agonistic interactions were observed during the study (Lazaro-Perea 2000). I further classified subordinate females into eldest subordinate female (always adult females) and other (adult and subadult) subordinate females. In five of the groups, the eldest subordinate female could be identified unambiguously due to known age or morphological characteristics and body size (although twins are common in this species, there was no other female of similar age as the eldest subordinate female in these groups). In group PB, however, there were several adult females of unknown age when we first started observing the group. Given that within-sex dominance is related to age in common marmosets (captive groups, Abbott 1984; wild groups, Digby 1995a), I used agonistic data to establish the most likely eldest females and classified two adult females as the eldest subordinate females in this group. In those groups in which the identity of the eldest female changed during the study period due to emigrations (groups E and Q), I used the longest period between emigrations for comparing the participation of subordinate females in intergroup interactions. I did not carry out similar analyses for subordinate males because only two of the groups had more than one subordinate male. I corrected individual frequencies of participation in intergroup interactions by dividing by the total number of intergroup interactions in which each group was involved. I analysed the participation of dominant and subordinate females, and of eldest and younger subordinate females in intergroup interactions using linear mixed-effects models on the raw or transformed data using group as a random effect. Data were arcsine squareroot transformed, as recommended by Martin & Bateson (1993) for data representing proportions, if residuals plots indicated problems with normality or heterogeneity of variances. When problems persisted after transformation of the data, I used permutation tests (with ‘Randibm’ programme, Edgington 1995), with 30 000 permutations per test. I used the SPlus library nlme (Pinheiro & Bates 2000) and SASs PROC MIXED (Little et al. 1996) for linear mixed-models, and SPlus v. 3.3 (Statistical Sciences 1995) for the rest of the analyses. I used paired sample tests (Wilcoxon matched-pairs signed-ranks tests or paired t tests depending on sample size) to compare (1) individual

differences in participation in chases against males versus females, (2) participation in intergroup encounters by the breeding pair depending on whether there was a same-sex individual in the other group and (3) participation in intergroup interactions by helpers depending on whether there were dependent infants in the group. I used Spearman’s rank correlations to analyse the relationship between participation in intergroup interactions by the breeding pair and the composition of their groups. I used Fisher’s exact tests for comparing the participation of male and female breeders in encounters with male and female intruders, and for analysing whether animals were more likely to participate in (1) forays into other groups, (2) extragroup sexual behaviour, and (3) nonaggressive approaches to animals from other group, depending on their status. All tests were two-tailed. RESULTS

Behavioural Patterns Observed during Intergroup Interactions I observed a total of 251 intergroup interactions during 1729 h of observation of the groups (averaging one intergroup interaction every 8.7 observation h, range 0.03– 0.36 intergroup interactions/h). The participants could be identified in 228 interactions. Intergroup interactions ranged in duration from 1 min to 4 h 17 min (median=17 min), and usually involved animals of only two different social groups (95%), although interactions involving three (N=7) and four (N=1) groups were also observed. The total number of animals involved in the interactions varied from two to 16 (median=6). Although most intergroup interactions involved more than one animal from each of two groups (defined as ‘intergroup encounters’), in 26.3% of the interactions (N=60), a single animal entered another group’s territory and interacted with animals from the group (defined as ‘intruder encounters’). The behavioural patterns most frequently observed during intergroup interactions and their frequency of occurrence are presented in Table 2. Ninety per cent of all intergroup interactions (94.1% of intergroup encounters and 76.7% of intruder encounters) included aggressive behaviour (chases, genital displays or contact aggression), but affiliative and sexual interactions between animals of different groups were also frequently observed (44.7% of intergroup encounters and 51.7% of intruder encounters). These included approaches to animals from the other group (in six of those cases, a male and a female from two different groups approached each other and one of them put its muzzle in close proximity to the back quarter of the other, as if sniffing it), with or without submissive vocalizations and sexual behaviour (copulations or attempted copulations). In 39% of intergroup interactions (40.5% of intergroup encounters and 35% of intruder encounters), I observed both aggressive and nonaggressive behaviour between animals of different groups within the same episode. Only 7.4% of intergroup interactions (4.2% of intergroup encounters and 16.7% of intruder encounters) were exclusively affiliative.

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ANIMAL BEHAVIOUR, 62, 1

Chases against extragroup animals

0.6

0.7 0.6

0.5

0.4

0.3

0.3

0.2 0.1 0

(a)

0.5

0.4

F

M

f

m

sb

Figure 1. Backtransformed adjusted means±SE proportion of chases against extragroup animals by animals of different status categories for groups E, E2, P, Q, M and PB when a reproductive female was present in the group. Proportions are calculated with respect to the total number of chases in which the group was involved as aggressor. Only those chases that occurred in the animals’ own territory are included. ANOVA on the arcsine squareroot transformed data: F4,30 =2.66, P=0.052. F=Breeding female, M=putative breeding male, f=subordinate/nonreproductive adult female, m=subordinate/nonreproductive adult male, sb=subadult.

Proportion of chases by group

Proportion of chases by the group

16

0.2 0.1 0 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

Most intergroup interactions among the study groups (75% and 79% for the forest and plantation groups, respectively) took place at the periphery of the home ranges, in areas of overlap between the home ranges of the groups involved. Among the two plantation study groups, the existence of a territory border was evident as most encounters occurred along the same 102 m imaginary band that separated both territories. That border, however, disappeared once group P was reduced to three individuals, and the larger group Q invaded, first partially and later completely, the old group P territory. Territory borders were more diffuse among the forest groups, but encounters occurred repeatedly in the same quadrants. Areas of conflict in the forest were characterized by a high density of fruit trees (80% of the fruit trees used by the marmosets were located in peripheral quadrants versus only 20% of the gum trees). Nevertheless, for most encounters it was not possible to determine whether the aggression was related to the use of any particular resource, and encounters still occurred in the home ranges’ periphery during the nonfruiting season. Both adult and subadult animals participated in encounters with other groups and single intruders. At least one subordinate individual participated in 98.5% of the intergroup and intruder encounters in their territory, and subordinate individuals chased extragroup animals away in 88.1% of the chases in which we could identify the aggressor (N=168; Fig. 1). In those chases in which the sex of the receiver could also be identified (N=110), there was evidence of sex specificity of chases (Fig. 2).

Participation of the Breeding Pair in Intergroup Interactions The participation of the reproductive female was highly variable among the groups, ranging from 21% of

(b)

Males Females Sex of the animal chased

Figure 2. Mean (±SE) proportion of chases against males and females in which (a) males and (b) females of the study groups were involved during intergroup interactions in their own territory. Proportions were calculated with respect to the total number of males and females that were chased by each individual’s group and comparisons were done within individual. Paired t test: males: t11 =3.05, P=0.011; females: t27 = −2.14, P=0.04.

interactions in group PB, to 73% in group E. There were no significant correlations between the reproductive female’s participation in intergroup interactions and group size (Spearman’s rank correlation: rS =
0.43, N=6, P=0.31), nor number of females in the group (Spearman’s rank correlation: rS =
0.64, N=6, P=0.14), but a marginally significant correlation with sex ratio (defined as number of adult females/number of adult males, Spearman’s rank correlation: rS =
0.79, N=6, P=0.07), indicating that breeding females were more likely to participate in intergroup interactions in those groups that had fewer females in relation to the number of males. The participation of putative breeding males was also highly variable, but in all groups exceeded 50% of intergroup interactions (range 54–91%). We found no significant correlations between participation of the putative breeding male and composition of the group (Spearman’s rank correlation: group size: rS =
0.23, N=6, P=0.56; number of females: rS =
0.18, N=6, P=0.65; or sex ratio: rS =0, N=6, P=0.95). When breeding females participated in intergroup interactions they were more likely to do so with the putative breeding male than by themselves (Wilcoxon matched-pairs signed-ranks test: T=2.1036, N=6, P=0.03). In intruder encounters, the sex of the intruder had an effect on the likelihood of participation of the breeding pair: breeding females participated in 10 of the 14

LAZARO-PEREA: INTERGROUP INTERACTIONS IN MARMOSETS

Table 4. Involvement in nonaggressive behavioural interactions with animals from other groups Number of animals involved in

Status

N

Forays into other groups

Extragroup sexual behaviour

Nonaggressive approaches

Breeding females Subordinate adult females Subadult females Putative breeding males Subordinate adult males Subadult males

6 15 7 6 5 1

0 7 3 1 4 0

0 8 1 2 2 0

0 11 5 1 4 1

intrusions by other females, but only in one of the 11 intrusions by males, whereas the values for the putative breeding males were six and seven, respectively (Fisher’s exact test: P=0.03). However, I found no effect of the sex of opponents in intergroup encounters. Breeding females were not more likely to participate in an intergroup encounter when there was at least one female in the other group (Wilcoxon matched-pairs signed-ranks test: T=11, N=6, P=1), and putative breeding males were not more likely to participate in an intergroup encounter when there was at least one male in the other group (T=0.9487, N=6, P=0.34). Reproductive females were never observed intruding into other group territories, following animals from another group, displaying or vocalizing submissively towards animals from other groups, or copulating with males from other groups. However, the putative breeding males of groups P and PB were involved in extragroup sexual behaviour with subordinate females of neighbouring groups in the midst of otherwise aggressive intergroup encounters (NPB =1, NP =2). Putative breeding males performed submissive approaches during intergroup encounters (PB) or as intruders in other groups (P). Interestingly, these were the two groups in which the reproductive female eventually died, but the intergroup interactions occurred months before her death.

Participation of Subordinate Animals in Intergroup Interactions Overall, subordinate adult females participated more often than the breeding females of their group in intergroup interactions in their own territory (ANOVA: F1,14 =8.41, P=0.01). However, when reproductive females did intervene in an intergroup interaction, they were equally as aggressive towards strangers as subordinate females in their groups, as indicated by their involvement in chases and lunges (randomization test: N=6 groups, P=0.4153). The involvement of subordinate animals in nonaggressive interactions with animals from other groups is presented in Table 4. Subordinate females were more likely than reproductive females to engage in extragroup sexual behaviour with males from other groups (Fisher’s exact test: P=0.04), to approach animals from other groups nonaggressively (Fisher’s exact test: P=0.001) and to intrude into other groups’ territories (Fisher’s exact

test: P=0.06). The same (marginally significant) trends were observed for males for forays into other groups and approaches to animals from other groups (Fisher’s exact test: P=0.08). Extragroup copulations, however, were equally divided between dominant and subordinate males (2 versus 2; Fisher’s exact test: P=1). Thirteen of 20 extragroup copulations or attempted copulations occurred during intergroup encounters that involved more than one animal from each of the groups, whereas in seven cases, one of the animals involved in the copulation (the female in four cases) entered the other group’s territory. In 55% of the extragroup copulations, at least one of the animals involved in the copulation had longcalled or scent-marked prior to copulating. In addition, most (15 of 20) of the intergroup interactions that included sexual behaviour also included aggressive behaviour between the animals of the two groups involved. Age and relative dominance status within the group influenced the participation of nonreproductive females in intergroup interactions. Eldest subordinate females were significantly more likely than younger subordinate females of their groups to participate in defence against other groups or against intruders (randomization test: N=5, P=0.026, after Bonferroni correction for multiple comparisons) and in extragroup copulations (randomization test: N=5, P=0.046, after Bonferroni correction for multiple comparisons). However, I found no significant differences in the frequency with which eldest versus younger subordinate females performed submissive behaviour to other groups (randomization test: N=5, P=0.48), tried to approach animals from other groups (randomization test: N=5, P=0.52), or intruded into other groups’ territories (randomization test: N=5, P=0.54). Interestingly, eldest subordinate females were not more likely to participate against female than against male intruders (Fisher’s exact test: P=1). Similarly, eldest helper females’ chases were directed equally against females and males during either intergroup or intruder encounters (Wilcoxon matched-pairs signed-ranks test: T=10, N=6, P=1).

Effects of Infant Births on Intergroup Interactions Infants were born in five of the groups, allowing us to investigate the potential effects of energetic constraints due to pregnancy, lactation and infant presence on the

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ANIMAL BEHAVIOUR, 62, 1

Proportion of intergroup interactions

18

0.5

0.4

0.3

0.2

0.1

Subordinate adult female Reproductive female Last trimester pregnancy + lactation

Other

Status of reproductive female Figure 3. Backtransformed adjusted means±SE proportion of intergroup interactions in natal territory in which reproductive and subordinate adult females participated as a function of reproductive status of the breeding female (ANOVA on the arcsine square-root transformed data: interaction: F1,16 =8.04, P=0.01).

participation of different group members. Reproductive females reduced their participation in defence during the periods of greatest energetic demands and mechanical constraints (last 2 months of pregnancy and lactation), whereas no changes were observed for subordinate females (Fig. 3). Participation in intergroup interactions by animals carrying dependent infants was rare but was observed in three of the four groups in which intergroup interactions occurred during the period of infant dependence (infants died in the fifth group, PB, during their first week). An animal carrying one or two infants participated in seven out of 44 (16%) possible intergroup interactions. More typically, animals carrying infants were not seen during intergroup interactions and I never observed all animals in a group participating in intergroup interactions when dependent infants were present. I found no significant difference in the frequency of participation of the putative breeding male and male and female helpers during those periods in which dependent infants were present and when there were no dependent infants in the groups (paired t test: t19 =0.99, P=0.33). DISCUSSION Intergroup interactions (including intruder and intergroup encounters) occurred almost daily in the study population. Aggressive behaviour was most frequently directed to same-sex individuals, and intergroup encounters occurred mainly in the periphery of the home ranges, suggesting that both mate defence and territorial defence were important functions of intergroup encounters. Furthermore, nonaggressive behaviour (most

frequently directed to opposite-sex individuals) were frequently observed during the same episodes as aggressive behaviour, and occurred during both intergroup and intruder encounters. Both breeders and helpers participated in intergroup interactions. Helpers were active in territorial defence, but their involvement in nonaggressive interactions suggests that assessment of breeding opportunities in neighbouring groups might also be occurring during intergroup interactions in the natal home range. Female (but not male) breeders showed sex-specific aggression against single intruders. Breeding pairs in captive settings show similar behaviour (Epple 1970; Harrison & Tardif 1989). This differential response to intruders might be related to the greater consequences of immigration by females into established groups, which are often associated with emigration or disappearance of all other adult females in the target group (Araujo 1996; Monteiro da Cruz 1998; see Baker & Dietz 1996 for similar results in wild golden lion tamarins). Male and female breeders also differed in their participation in nonaggressive interactions with animals from other groups. Putative breeding males in two groups were seen directing nonaggressive behaviour (including copulations) towards females in other groups. These two males were the partners of the two reproductive females that subsequently died. As has been reported for whitehanded gibbons, Hylobates lar (Reichard 1995), our data suggest that those extragroup copulations could be related with assessment of potential future partners (see below) for males mated with old or unhealthy reproductive females, which might have low remaining reproductive tenure. Incorrect assignment of males to the putative breeding male category in one of the groups (in the other there was only one adult male) also needs to be considered as a potential cause of this result. In contrast, none of the reproductive females were seen approaching or engaging in sexual behaviour with males from other groups. Our results differ from Digby’s (1999) study of three polygynous groups in the same population. She observed both male and female breeders engaging in extragroup copulations. Due to competition for helpers and the potential threat of infanticide (Digby 1995b), sharing reproduction with another female within a group might not be as good a strategy for a female as being the single breeder in another group. Therefore, females in polygynous groups might still benefit by assessing possibilities in other groups. In Digby’s (1999) sample, the group that was monogamous for most of the study was also the one in which the breeding female was not seen to engage in extragroup copulations, supporting the interpretation that reproductive strategies of breeding females in monogamous and polygynous groups differ. Breeding females decreased their involvement in intergroup interactions during periods of high energetic demand, and animals carrying infants were rarely seen participating in intergroup encounters. Although we cannot calculate the exact costs of participation in intergroup interactions for different individuals, involvement in aggressive interactions is potentially costly in terms of energy expenditure, risk of injury from conspecific

LAZARO-PEREA: INTERGROUP INTERACTIONS IN MARMOSETS

aggression, and exposure to predators due to increased conspicuousness and decreased agility. These costs are probably higher for the breeding female and for the animals carrying infants, due to the high energetic demands of pregnancy and lactation and the mechanical constraints during the last part of pregnancy and while carrying infants. In this context, participation of helpers in territorial defence provides obvious benefits for the breeders if it decreases the costs of defence for the breeding animals. This suggests that territorial defence constitutes an important contribution by helpers in wild groups of common marmosets, and that the presence of helpers allows the breeding female and infant carriers to reduce their participation in intergroup interactions, therefore decreasing the costs of territorial defence. Observations on the involvement of breeding females in groups with no helpers (not available in our sample) would be necessary to test this assertion. Why should helpers be actively involved in territorial defence? Benefits to nonreproductive individuals could be either indirect (i.e. increase their inclusive fitness by way of improving the reproductive success of their relatives) or direct. Possible direct benefits could include protecting their position in the reproductive queue by not allowing the immigration of new animals into the group. Eldest adult subordinate females would have more to lose if an adult female immigrated into the group. Eldest adult subordinate females were more involved in defence against extragroup animals than younger (adult and subadult) subordinate females, supporting the prediction that relative position in the reproductive queue affects participation in territorial defence. Nevertheless, due to the limitations of the data set (only broad age estimations were used for most females, both adult and subadult females were grouped as ‘younger’ subordinates, and agonistic data was used to establish the eldest females in one of the groups) this remains as a preliminary analyses and further data on females of known age are needed to establish more solidly how participation in intergroup encounters varies with age. Additional benefits to helpers become apparent when we consider that neighbours are not only competitors, but also potential mates. Zahavi (1974, 1995) suggested that helping behaviour directly benefits helpers by sending information about individual quality and thus increasing their ‘social prestige’. By showing off how much they can invest in cooperation with other group members, animals display their ability to win a fight and their desirability as groupmates. Participation in intergroup aggression is witnessed not only by groupmates, but also by animals of neighbouring groups. Thus, by participating in territorial defence, helpers might be displaying their quality to their groupmates and to potential mates in neighbouring groups. The idea that animals gain information by observing fights among others is not new. Experiments on redwinged blackbirds, Aegalaius phoeniceus (Freeman 1987) showed that territorial males regulated their likelihood of intrusion into neighbouring territories depending on the observed response of the resident to other intruders. Similarly, Oliveira et al. (1998) showed that males of the

fish Betta splendens monitor aggressive interactions between neighbouring conspecifics and use that information in subsequent encounters with the males. Whether information gathered through monitoring aggressive interactions by potential immigrants affects the immigration process in common marmosets (or other cooperative breeders) would be difficult to test with observational data. However, experiments in captivity could be designed to address this question. The involvement of helpers in nonaggressive interactions with animals of other groups also suggests that assessing and establishing nonaggressive contact with neighbours are important functions of many intergroup interactions. Common marmoset helpers made forays into other groups. During these forays, animals often directed nonaggressive behaviour towards animals from the other groups, approached them submissively and engaged in sexual behaviour with them. I observed similar behaviour (submissive approaches, inspection of intruders and extragroup copulations) by subordinate animals in the midst of aggressive intergroup encounters in their territory, suggesting that assessment of neighbours might not only be accomplished during individual forays into neighbouring territories, but during intergroup interactions in the helpers’ home range as well (see also Buchanan-Smith 1991; Garber et al. 1993; Goldizen et al. 1996). Furthermore, the fact that about half of the instances of extragroup sexual behaviour were preceded either by long calling or by scent marking suggests that animals are not trying to be cryptic, but are advertising their presence to (most probably) opposite-sex animals from another group. Through these intergroup interactions, nonreproductive animals might gather information about the group composition, assess the existence of a breeding vacancy, and gauge the neighbouring group’s response to a potential immigrant (see Perry 1996, for a similar interpretation of nonaggressive interactions by subordinate male white-faced capuchins, Cebus capucinus, during intergroup encounters). Furthermore, repeated interactions with the same individuals and engagement in sexual behaviour might function to reduce the aggression received when attempting to immigrate. Intruder studies in captive Wied’s black-tufted-ear marmosets have shown that familiarity reduces the amount of aggression that an intruder receives (French et al. 1995), and gradual exposure facilitates social acceptance of captive male rhesus monkeys, Macaca mulatta, into a female group (Tannenbaum 1997). In addition, sexual activity stimulates oxytocin release in many species including primates (Carter 1992), and oxytocin has been related to establishment of social bonds between males and females in some rodent species (Insel 1992). In summary, common marmoset helpers cooperate in territorial defence and their help might decrease the costs of defence for the reproductive animals. The involvement of subordinate females in nonaggressive behaviour towards members of other groups suggests that intergroup interactions in the natal home range are used, together with forays into other group territories, to evaluate potential reproductive opportunities in other groups. These data contribute to an understanding of the

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ANIMAL BEHAVIOUR, 62, 1

behavioural mechanisms used for dispersal decisions and mate choice in a cooperatively breeding species, but similarly detailed field data and experiments in a captive setting will be valuable to establish the generality of these results and to test several of the hypotheses proposed here. Acknowledgments I want to thank IBAMA and the Departamento de Fisiologia da Universidade Federal do Rio Grande do Norte and especially M. Fa´ tima Arruda and M. Bernardete C. de Sousa for granting permission to carry out this study and for providing logistic support. Fabi´ola Alburquerque and Edinaldo Nascimento helped with capturing the monkeys. Simone Porfirio de Souza and Maria Carla Lopes de Nascimento provided invaluable help in data collection and habituation of one of the groups. Ramo´ n Di´az-Uriarte provided statistical advice and logistic support during all parts of the study. I want to thank the members of my graduate committee D. H. Abbott, J. R. Baylis, C. A. Marler, K. B. Strier and especially C. T. Snowdon for their support and advice. I thank Carol M. Berman, Anne A. Carlson, Ramo´ n Di´az-Uriarte, Anita J. Ginther, Catherine A. Marler, Susana Sa´ nchez, Charles T. Snowdon, Karen B. Strier, Suzette D. Tardif, Toni E. Ziegler and two anonymous referees for their comments on the manuscript. Funds were provided by the National Geographic Society (grant to C. Lazaro-Perea and C. T. Snowdon), NIMH (grant MH 35,215 to C. T. Snowdon), University of Wisconsin Graduate School (grant to C. Lazaro-Perea), and the Wisconsin Regional Primate Research Center (grant RR 00,167). The research presented here was approved by the Animal Care and Use Committee of the University of Wisconsin (Animal Research Protocol A-48-7400-L00030, approved in February 1996). This project was carried out under an agreement of cooperation between the Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte, Brazil and the Department of Psychology, University of Wisconsin-Madison, U.S.A., and all procedures used in the study complied with Brazilian laws and were approved by CNPq. This is publication 40-008 of the WRPRC. References Abbott, D. H. 1984. Behavioural and physiological suppression of fertility in subordinate marmoset monkeys. American Journal of Primatology, 6, 169–186. Anzenberger, G. 1985. How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: the quality of behavior. Folia Primatologica, 45, 204–224. Araujo, A. 1996. Influence des facteurs ecologiques, comportementaux et demographiques sur la dispersion de Callithrix jacchus. Ph.D. thesis, Universite Paris-Nord (Paris XIII). Araujo, A., Arruda, M. F., Alencar, A. I., Alburquerque, F., Nascimento, M. C. & Yamamoto, M. E. 2000. Body weight of wild and captive common marmosets (Callithrix jacchus). International Journal of Primatology, 21, 317–324.

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