HOW ADAPTIVE OR PHYLOGENETICALLY INERT IS PRIMATE SOCIAL BEHAVIOUR? A TEST WITH TWO SYMPATRIC COLOBINES by AMANDA H. KORSTJENS 1,2,4,5) , ELISABETH H.M. STERCK 1) and RONALD NOË3,4,5,6) (1 Behavioural Biology group, Utrecht University, Padualaan 14, PO box 80.086, NL-3508 TB Utrecht, The Netherlands; 3 Ethologie et Ecologie comportementale des Primates, CEPE (CNRS UPR 9010), Université, F-67000 Strasbourg, France; 4 Taï Monkey Project, CSRS, Abidjan, Côte d’Ivoire; 5 MPI Seewiesen, Starnberg, Germany) (Acc. 30-XI-2001)

Summary Socio-ecological theories predict that females adapt their social behaviour to their environment. On the other hand, as a result of phylogenetic inertia, social behaviour may be slow to catch up when the environment changes. If social behaviour is adapted to the environment, competition and co-operation among females is predicted to re ect the characteristicsof food sources. Contest competition both between and within groups is expected to result in alliances among related, philopatric, females. We compared social relationships and food characteristics of two sympatric and congeneric primate species, the red colobus and the black-and-white colobus of the Taï National Park, Ivory Coast. We found that afŽ liative interactions among females were comparable between the species. The differences in food characteristics could explain why black-and-white females competed more often than did red colobus females,

2)

Corresponding author’s e-mail address: [email protected] We thank the ‘Ministère d’Enseignement Supérieur et Recherche ScientiŽ que’, the ‘Ministère d’Agriculture et Resources Animales’, the ‘Centre Suisse de Recherche ScientiŽ ques’, the ‘P.A.C.P.N.T.’ and the ‘Centre de Recherche en Ecologie’ in Côte d’Ivoire for support and permission to conduct research in the Taï National Park. The research was Ž nancially supported by the ‘Max-Planck Institut für Verhaltensphysiology’, the ‘Deutsches Forschungs Geselschaft’, the ‘University of Utrecht’ and the ‘Lucie Burgers Stichting’. We thank Estelle Nijssen, Boris van Oirschot, Romain Blé, Ferdinand Bélé and Bertin Diero for their assistance in the Ž eld and Estelle Nijssen and Boris van Oirschot for their share in the data processing. We further thank Jan van Hooff, Eleni Nikitopoulos, Phyllis Lee, Lynne Isbell, and Joan Silk for their valuable comments on earlier drafts of the manuscript. 6)

© Koninklijke Brill NV, Leiden, 2002

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both at the intra- and inter-group level. In contrast to socio-ecological theory, female intergroup aggression was not linked to female philopatry in black-and-whitecolobus. The species differed from each other and from other populations of the same or closely related species with respect to their inter-group behaviour which indicates that phylogenetic inertia did not constrain this aspect of social behaviour. Keywords: intra-group and inter-groupsocial relationships,socio-ecologicalmodel, afŽ liative and agonistic interactions among females, western red colobus, western black-and-white colobus.

Introduction Group living and alliances are important aspects of primate social behaviour. We assume that diurnal primates live in groups either as a result of conspeciŽ c competition over food (Wrangham, 1980; Isbell, 1991) or for protection against predators and/or infanticidal conspeciŽ c males (van Schaik, 1983, 1996; Noë & Bshary, 1997). Furthermore, the spatio-temporal distribution of key food sources is expected to determine the pattern of competition among females of the same and different conspeciŽ c groups (e.g. Janson, 1988; van Schaik, 1989; Milinski & Parker, 1991; van Hooff & van Schaik, 1992). Females are expected to form alliances at the level that yields the highest net beneŽ t for the individuals involved when contest competition among females is strong and food sources can be shared among alliance partners. An alternative view emphasises the role of phylogenetic inertia (Thierry, 1990; Di Fiori & Rendall, 1994; Thierry et al., 2000). The stronger the inertia the less some of the present-day primates are adapted to their present-day environment and the more variation between species is explained by their phylogenetic distance. In order to test if the social behaviour of females of two sympatric colobus species was adapted to their environment or not, we investigated their social behaviour and characteristics of the food they selected. The ‘socio-ecological model’ (Wrangham, 1980; van Schaik, 1989; Isbell, 1991; Sterck et al., 1997; Isbell & Young, this volume), which is based on the assumption that behaviour is adaptive, yields the following predictions: When key food items can be monopolised by single individuals, intragroup contest competition is strong, which leads to strongly asymmetrical dominance relationships. Individuals are expected to form alliances in order to overcome the disadvantages of subordinance. On the basis of kin selection theory we expect most alliances to be formed among related individuals,

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which in turn forces females to remain with their kin, in other words to be philopatric. Food sources, such as fruit trees, can also be large enough to feed a whole group and small enough to be defended against other conspeciŽ c groups. In that case we expect alliances at the group level and a relaxation of the intra-group contest competition in order to preserve the more important group-level alliance (van Hooff & van Schaik, 1992). When neither form of contest competition is strong, females have little to gain from philopatry and are expected to migrate when this has important beneŽ ts to them (e.g. inbreeding avoidance, avoidance of intra-group competition, or reduction of male harassment). This hypothesis is refuted if we Ž nd populations or species in which the characteristics of the environment and the characteristics of the social behaviour don’t Ž t together. One major difŽ culty in testing the socio-ecological model is the problem of how to deŽ ne a ‘monopolisable patch’. Isbell et al. (1991) argue that the longer individuals spend in a certain patch, the likelier it is that they will contest access to it. They argue that this ‘food patch residence time’ is affected by the size of food items, the handling time per food item and the number of individuals in the same patch relative to the size of the patch. When many animals forage in a given patch with small items which require little processing, the quality of a food spot decreases rapidly per unit time. When an item requires a long processing time, and possibly processing skills, the quality of the spot increases per unit time until the desired part of the food item has been obtained. Therefore, contest competition is expected to be especially high in food patches with long residence times and long handling times. Handling time, food patch residence time, food patch size and number of foragers per patch can be measured more directly than distribution and abundance of food. The more strongly phylogenetic inertia constrains behaviour in primates (Thierry, 1990; Di Fiori & Rendall, 1994; Thierry et al., 2000), the less some of the present-day primates are adapted to their present-day environment and the more variation between species is explained by their phylogenetic distance. Related species are expected to show very similar behavioural patterns (which re ect adaptations to the environment of the parent species of the clade). This hypothesis can be rejected when we Ž nd closely related species that live in different environments and exhibit social behaviour that is adapted to their speciŽ c environment.

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The word ‘environment’ used in these hypotheses is equivalent to the ‘niche’, the set of elements in the natural world that are relevant to an individual’s Ž tness. A single tropical forest, for example, has many different niches to which different species are adapted. Different niches act as separated ‘environments’, even if they are physically intertwined in the same forest, when adaptations of an anatomical or physiological nature prevent a species from utilising resources outside its ‘niche’. Inter-speciŽ c comparisons are strong tools in testing the validity of socioecological models or the effect of phylogenetic inertia (e.g. Mitchell et al., 1991; Barton et al., 1996; Sterck & Steenbeek, 1997; Isbell & Pruetz, 1998; Isbell et al., 1998, 1999; Thierry et al., 2000). In this paper we compare two sympatric congeners, the western red colobus monkey (Procolobus badius badius) and the western black-and-white colobus monkey (Colobus polykomos polykomos). Each species occupies a different niche in the same tropical forest, the Taï National Park in Ivory Coast, which gives us a chance to test the two hypotheses outlined above. Red colobus live in large multi-male, multi-female groups consisting of 30-90 individuals (Struhsaker, 1975; Struhsaker & Oates, 1975; Galat & Galat-Luong, 1985; Bshary & Noë, 1997b; Höner et al., 1997; Korstjens, 2001b). Females disperse and males are philopatric or return after a solitary period to their natal group (Struhsaker & Oates, 1975; Struhsaker & Leland, 1979; Struhsaker, 1980; Galat & Galat-Luong, 1985; Bshary & Noë, 1997a, b). Males of red colobus groups defend territories or their females against foreign males (B. Beerlage, unpubl. data), whereas females do not participate in inter-group aggression (Clutton-Brock, 1975; Struhsaker & Leland, 1979). Red colobus monkeys are foli-frugivores (Struhsaker, 1980; Marsh, 1981; Wachter et al., 1997; Davies et al., 1999; Korstjens, 2001c). Compared to the black-and-white colobus of Taï they exploit relatively abundant and evenly distributed food sources (Korstjens, 2001c). On the basis of their food characteristics, dispersal system and inter-group relationships, the socio-ecological models predict that female red colobus have little intragroup food competition and few afŽ liative interactions. Black-and-white colobus live in polygynous groups consisting of 14-19 individuals (Galat & Galat-Luong, 1985; Dasilva, 1989; Korstjens, 2001b). Data indicate that both males and females may disperse (Dasilva, 1989; Korstjens, 2001c), as in the black colobus (C. satanas: Oates, 1994), but in contrast to eastern black-and-white colobus (C. guereza: Dunbar &

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Dunbar, 1974; Oates, 1977). In Taï, the home ranges of black-and-white colobus groups overlap extensively (Korstjens, 2001a). In most populations of black-and-white colobus females rarely if ever participate in inter-group aggression (Oates, 1977; Struhsaker & Leland, 1979; Fashing, 2001a, b). Like the red colobus, black-and-white colobus are foli-frugivores, but their diet overlaps only slightly with that of the red colobus (Davies et al., 1999). Their food sources, however, are relatively more clumped (Korstjens, 2001a). Another important difference between the two species is the time they spend in poly-speciŽ c association. The red colobus groups each have a particular Diana monkey partner group and associate with Diana monkey groups more than expected by chance, in contrast to the black-and-white colobus groups who are rarely in found in poly-speciŽ c associations. Here we compare social behaviour and food characteristics for the two species in order to test in how far phylogenetic inertia or adaptations to the environment have affected the social behaviour of the species.

Methods The study site This study was carried out in the Taï National Park (between 6± 200 N to 5± 100 N and 4± 200 W to 6± 500 W), Ivory Coast. The forest has been classiŽ ed as a tropical evergreen seasonal lowland forest (Stoorvogel, 1993). Details of the study site are published elsewhere (Galat & Galat-Luong, 1985; Boesch & Boesch, 1989; Bshary, 1995; McGraw, 1996; Boesch & Boesch-Achermann, 2000). The study groups Behavioural data were collected on red colobus group Bad2A. This group was the largest daughter fraction of group Bad2 that split up at the start of the study. Bad2A group consisted of approximately 60 individuals. It contained on average 12 identiŽ ed adult and 2 identiŽ ed sub-adult males, 20 individually recognised and 1-3 unidentiŽ ed adult females, 1 known and 1-2 unidentiŽ ed sub-adult females, and approximately 13 juveniles and 8 infants. Recognition was based on characteristics of the face and tail and on skin colouring of inner-thighs. Kin relationships were not known. Data on between group interactions stem from both daughter fractions of former group Bad2 (Bad2A & Bad2B, §60 & 44 individuals respectively) and from the two daughter fractions of former group Bad1 (Bad1A & Bad1B, §41 & 64 individuals respectively; van Oirschot, 2000). The data on diet, food patch size, day journey length, distance travelled per hour, and home range size were collected on Bad2 without distinguishing between the groups A and B because groups were regularly intermingled at the start of the study. Data of the black-and-white

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colobus stem from group Pol1. This group contained 1 adult male, 4 sub-adult and 5 adult females, 2 juvenile males and 2-5 infants until February 1998 (i.e. period 1). At the beginning of February 1998 three sub-adult females (females Mo, Ky & Mi) disappeared. The period between February 1998 and September 1998 was indicated as period 2. All individuals were recognised on the basis of facial and tail characteristics. Some individuals were known to be related: Ta is the mother of sub-adult female Tu, Ma is the mother of sub-adult female Mi, and Ka is the mother of sub-adult female Ky. Group composition and size of the study groups were representative for the population (Galat & Galat-Luong, 1985; Korstjens, 2001c). For the red colobus group data were collected on 16 individually recognised adult females. For the black-and-white colobus group data were collected on Ž ve adult and four sub-adult females. The latter category was used for females that were likely to be sexually mature, but who were nulliparous and still visibly smaller than adult (parous) females. Sub-adult females were included in the analyses because statistical comparisons between the species would have been impossible when excluding the sub-adult females of Pol1. Data collection The study was conducted from January 1997 through December 1998. Most data were collected during full day follows of the groups. The same criteria were used for both species. Scan samples (Martin & Bateson, 1993) were taken every hour and lasted for a maximum of 25 minutes. The observer assured that no single individual was sampled twice during this time on the basis of individual recognition and location in the group. For each scanned individual observers noted: the age-sex class, identity, activity (lasting for at least 5 seconds), item consumed, the nearest adult or sub-adult male and female and the diameter at breast height (‘DBH’) and species of the tree in which a foraging animal was located. The activities scored were resting (including auto-grooming); foraging (any activity that concerned the handling or eating of food); moving; allo-grooming; and other (which was mainly sexual behaviour). Data on time spent with a neighbour are derived from ‘neighbour’-scan samples collected by one observer (AHK). She collected 991 samples of 16 red colobus females and 153 samples on 6 black-and-white colobus females (only during period 2). A ‘neighbour’ is an adult or sub-adult individual located within two meters of the subject of the scan sample. The time spent with neighbours was measured as the percentage of scans in which a certain female had at least one neighbour. Wilcoxon matched pairs signed ranks tests (paired for individual females) and Mann-Whitney U -tests (for comparisons between the two species) were performed with the individual animal as the sampling unit. The neighbour data are presented in two ways: (1) as the percentage of the total number of scan samples of a female in which she had any adult female or male within 2 m distance (the uncorrected percentage); and (2) as this percentage for distances among females corrected for the sex ratio in the group (the corrected percentage). The corrected percentage was calculated by multiplying the uncorrected female-female percentage by 0.5 (red colobus) and 0.17 (black-and-while colobus). The percentage of female-male proximity did not require correction. Dietary data were derived from ‘food’-scan samples collected by four observers. The diet is expressed as the percentage of scans (for Bad2: 5910 and for Pol1: 3091 scan samples) in which a certain food item was consumed. For the dietary data no distinction was made between ‘whole fruits’ and ‘seeds’. Food tree size is obtained from the median of all scan samples in which the DBH of the tree was measured (for Bad2: 3951 and for Pol1: 1878 samples of trees).

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Focal animal samples (Martin & Bateson, 1993) lasted from three to ten minutes. Consecutive focal samples of the same individual were separated by at least one hour. One observer (AHK) collected 21.3 hours of observation on 16 females of Bad2A. Two observers (AHK and Estelle C. Nijssen, ‘ECN’) collected 118 hours of observation on 9 females of Pol1 (unless mentioned otherwise). During a focal animal sample social interactions (see below) involving the focal individual were recorded continuously. Data on the activity of the individual were collected with the instantaneous method at one-minute intervals. The number of times an individual moved its arm in order to pick a food item and the number of movements of an individual were recorded. The number of arm movements, used as an indication of handling time of food items, was calculated per minute and averaged per focal sample (for Bad2A: 60; and for Pol1: 60 samples). Mann-Whitney U -tests were done using the focal sample as sampling unit. The ‘food spot residence time’ was deŽ ned as the number of full minutes a foraging animal did not move more than 50 cm. In the special situation when animals moved with the food item in hand we did not measure this as the desertion of a food spot (this applied only for woody pots eaten by black-and-white colobus). A new sample was started for each new patch an individual visited. Since focal samples maximally lasted ten minutes, some of the food spot residence periods were truncated (‘censored’ data) when the focal ended but the individual still foraged in the same spot. Therefore, we used Kaplan Meier tests of survival, in the loglinear analysis setting (from the SPSS 7.5 for windows program) to compare food spot residence time between the species. On Bad2A we collected 82 non-censoredand 47 censored samples; for Pol1 we collected 59 non-censored and 53 censored samples. Data of food spot residence time and handling time were collected by one observer (AHK). These data were too scarce for individual-basedtests. For the purpose of analyses we assigned food items into Ž ve categories: leaves,  owers, whole fruits, seeds and other. ‘Whole fruits’ were those fruits for which the skin,  esh or entire fruit were consumed. ‘Seeds’ were those fruits for which only the seeds were consumed. Ad libitum data on agonistic behaviour and grooming (Martin & Bateson, 1993) were collected by one observer (AHK) for red colobus and two observers (AHK & ECN) for blackand-white colobus. Data on the distance travelled per hour or per day were derived from hourly samples of the location of the centre of the group in relation to a painted grid system with 100£ 100 m cells. During 190 days for Bad2A and during 309 days for Pol1 we measured on average 8.5 hourdistances. Data were collected by a total of Ž ve observers (including AHK and ECN). Inter-group interactions were recorded when individuals of different groups approached each-other to within 50 meters. Data on inter-group encounters were collected on the ‘sistergroups’ (Bad1A, Bad1B, Bad2A and Bad2B) of the former groups Bad1 (two observers) and Bad2 (observer AHK) and on Pol1 (observers AHK and ECN). The red colobus ‘sistergroups’ still shared a home range and a Diana monkey partner group during this study. Social interactions Agonistic interactions included all instances of submissive and/or aggressive behaviour. Submission was recorded when one individual yielded to,  ed from, or crouched in front of another individual. Aggressive actions included threatening, pushing, biting, hitting, chasing, and stealing food from an individual. Nearly all of the aggressive acts produced a submissive response. When several agonistic or submissive acts occurred in the same context within

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3 minutes of each other, all of the events were considered to be part of a single interaction. For the purpose of analysis, we identiŽ ed three contexts in which agonistic interactions occurred. When the approached or aggressed individual was foraging, the context was labelled as ‘food’; when two individuals contested access to an infant, the context was ‘infant’; and in all other instances the context was ‘other’. A dominance hierarchy was constructed with the Matman program (de Vries et al., 1993). A coalition was recorded when two individuals simultaneously threatened or chased a third individual. A single grooming bout was deŽ ned as series of grooming episodes between the same individuals with interruptions of less than three minutes. When two individuals groomed alternately this was recorded as one event for each individual, irrespective of how often the direction switched during the grooming bout. General data analyses Scan and focal data of individuals were used when ten or more samples or minutes were available. Non-parametric statistics were used. All tests are two-tailed and ® is set at 0.05. An ® 0 value was calculated using a ‘sharper Bonferroni correction’ method when multiple tests were performed with the same dataset (Hochberg, 1988). Tests on data collected by several observers were only used when inter-observer reliability was more than 90%. The boxplots as depicted in the Ž gures always represent the quartiles of the samples, with minimum and maximum values, plus extremes and outliers and they were obtained with the program SPSS 7.5 or 9.0 for Windows.

Results Female red colobus Diet choice and handling time of food items Food competition is expected to depend on the time that individuals spent in a food patch and the quality of the food patch. These factors can be measured from diet choice, food patch size, handling time and food spot residence time. Red colobus monkeys visited relatively large trees with a median DBH of 51 cm. Their diet consisted for 43% of leaves, 33% of fruits, 23% of  owers and 1.0% of termites (N D 5910 scan samples). We measured whether handling time differed between food items (Mann-Whitney U -test: Nseeds D 11, Nfruits D 4, Nleaves D 25, N owers D 15; seeds — whole fruits: U D 8:5, p D 0:068; seeds — leaves: U D 108:5, p D 0:31; seeds —  owers: U D 66:0, p D 0:37; leaves —  owers: U D 186:0, p D 0:016, ® 0 D 0:017; Fig. 1). Similarly, no signiŽ cant difference between food items was found for the ‘food spot residence time’ (Kaplan Meier test: statistic 7.23, df D 4, p D 0:124). Thus, food spot quality in red colobus depended little on the items consumed.

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Fig. 1. The average number of arm movements per minute while foraging on different food items for red and black-and-white colobus; depicted are quartile values per item of average number of arm movements per food patch, ‘N ’ D number of food patches for which data were available, circles represent outliers and asterixes represent extremes of the samples; ‘Fruits’ refers to those fruits for which either the  esh, skin or the entire fruit was consumed, ‘seeds’ refers to those fruits for which only seeds were consumed. The category ‘other’ consists mainly of insects. Pol1 and Bad2A are the study groups of black-and-white and red colobus respectively from which data were obtained.

Female dispersal and female inter-group aggression We encountered 12 solitary juvenile or sub-adult red colobus individuals in association with black-and-white colobus groups. Of these individuals three were probably female and nine were certainly males. Only one female immigration (into group Bad1) was observed. This lack of observations on female dispersal was probably due to the large size of the groups and the lack of individual recognition by most observers of these monkeys. Inter-group encounters between sister-groups were common: Bad1A and Bad1B encountered each other once every 3 days (122 observation days), and Bad2A and Bad2B encountered each other once every 2 days (63 obser-

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vation days). Of these inter-group encounters 4% (Bad1A and B) and 29% (Bad2A and B) involved aggressive chases or physical contact. Inter-group encounters with non-sister groups were rare: one every 30 days for Bad1A and B (122 observation days); one every 21 days for Bad2A and B (63 observation days). Aggression occurred in two out of four (Bad1) and one out of three (Bad2) of these inter-group encounters. A few females were observed to join males in threat displays in three of the eight aggressive encounters between Bad2A and Bad2B. Females were passive in all other recorded intergroup encounters. Intra-group interactions by females Aggressive interactions among females were uncommon, 0.19 interactions per focal observation hour, and were especially frequent in the context of foraging: three of the four interactions that occurred during focal follows involved food, 0.65 interactions/hour spend foraging. Aggression among identiŽ ed females was too infrequent (4 interactions in 21.3 hours of focal observations and 8 when ad libitum data were included), to construct a dominance hierarchy or to test different rates of aggression for different food items. In one of the eight aggressive interactions among females a coalition was formed (one in 21.3 focal observation hours). This interaction occurred when a female approached two resting females. Although females spent as much time near sub-adult or adult males as they spent near other sub-adult or adult females (Fig. 3; uncorrected percentages Wilcoxon matched pairs signed ranks test z D ¡0:126, p D 0:900, ® 0 D 0:025), they had males as neighbours more often than expected on the basis of group composition (corrected percentages: Wilcoxon matched pairs signed ranks test z D ¡2:954, p D 0:003, ® 0 D 0:025). The females seemed to groom individuals of both sexes about equally often: 0.94 ‘female grooms female’ interactions per focal observation hour and 1.02 ‘female grooms male’ interactions per hour. The data from scan and focal samples were too scarce to allow a statistical analysis on the preference of females to groom either males or females. An analysis of the ad libitum data revealed that females groomed other females as often as they groomed males (uncorrected percentages: Wilcoxon matched pairs signed ranks test z D ¡0:84, p D 0:4, ® 0 D 0:025), whereas the corrected percentages showed that females tended to prefer males over females (comparison of corrected percentages: Wilcoxon matched pairs signed ranks test z D ¡1:86, p D 0:06, ® 0 D 0:025).

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Female black-and-white colobus Diet choice and handling time of food items Black-and-white colobus foraged in trees with a median DBH of 47 cm. They consumed leaves 42%, fruits 56%,  owers 2% and insects less than 0.05% of their foraging time (N D 3091 scan samples). The average number of arm movements per patch visit was higher when females consumed whole fruits or leaves than when they consumed seeds (Mann-Whitney U -test: Nseeds D 24, Nfruits D 8, Nleaves D 23; seeds — fruits: U D 9:0, p D 0:000; seeds — leaves: U D 22:5, p D 0:000; fruits — leaves: U D 87:0, p D 0:82, ® 0 D 0:025). The food spot residence time differed between the different classes of food items (Kaplan Meier loglinear test: statistic D 7:08, df D 2, p D 0:0291). This difference was signiŽ cant due to the difference between whole fruits and leaves (same test df D 1: fruits — leaves: statistic D 6:3, p D 0:012; fruits — seeds: statistic D 2:69, p D 0:10; seeds — leaves: statistic D 2:17, p D 0:14; ® 0 D 0:017, Fig. 1). Female dispersal and female inter-group aggression Two parous females (females Ir and Ta) immigrated into group Pol1. One female (Ir) might have been the same individual that disappeared a year earlier when identiŽ cation of individuals was still difŽ cult. Three sub-adult females in the group disappeared simultaneously in February 1998. All three females appeared to be in good health and were not the most peripheral or most vulnerable individuals in the group. Unfortunately we did not Ž nd the females in any of the 4 neighbouring groups that we visited afterwards. Thus, two (Ta & Ir) of the Ž ve parous females were not natal and only one (Tu) of the four natal females bred in her group. Female Tu was was most likely conceived previous to the immigration of her mother Ta into Pol1. Inter-group interactions occurred once every Ž ve days (20 interactions in 99 observation days). Contact aggression between members of different groups was observed in 35% (N D 7 interactions) of the inter-group interactions. The dominant resident male was always involved in aggression or threat displays and he was joined by at least one female in 57% of these encounters. In each of the latter cases more than one female was involved.

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Intra-group interactions by females Agonistic interactions were relatively common among black-and-white colobus females (0.60 interactions per focal observation hour). Most aggressive interactions took place in the context of foraging: 1.58 interactions concerning food/hour spend foraging and 0.23 interactions not concerning food/hour spend on non-foraging activities (Wilcoxon signed ranks test: N D 9 females, z D ¡2:67, p D 0:008). There was a relationship between the food item category (seeds, whole fruits or leaves) and the frequency of agonistic interactions (Friedman test N D 8 females,  2 D 8:6, df D 2, p D 0:014). Most agonistic interactions occurred when the females were foraging on seeds, but only the post-hoc test between the two extremes: whole fruits versus seeds was signiŽ cant (Wilcoxon signed ranks tests: seeds — leaves: 9 females, z D ¡1:13, p D 0:260; seeds — fruits: 8 females, z D ¡2:38, p D 0:017; leaves — fruits: 8 females, z D ¡1:69, p D 0:091; ® 0 D 0:017). Thus, agonistic interactions appear to correlate more strongly with handling time per food item, which was shortest for whole fruits and longest for seeds, than with food spot residence time, which was shortest for leaves and longest for whole fruits. Data on handling time and food spot residence time were too few to do the correlation that is required to test this more strongly. A linear dominance hierarchy could be constructed for the period before the sub-adult females disappeared (Table 1; Lindau’s linearity index h D 0:83, p D 0:0005). However, 13% of the submissive actions were directed at a subordinate individual. There was no apparent relationship between female reproductive success, measured as the inter-birth interval (after an offspring survived to an age of one year) and dominance rank. None of the 4 mother-daughter pairs occupied adjacent ranks (Table 1). We observed no female coalitions in 123 agonistic interactions. We did observe once that a daughter (Tu) came to the aid of her mother: the mother, who was carrying a young infant, was being attacked by the adult male and the daughter relieved her mother of the infant after which the mother could  ee more easily. (The male was apparently interested in having a sexual interaction with the mother, not in attacking the infant.) Although females tended to spend more time near another female than near the male (Fig. 3; uncorrected percentages: Wilcoxon matched pairs signed ranks test z D ¡2:00, p D 0:046), females did not preferentially seek the company of other females (corrected percentages: Wilcoxon matched pairs signed ranks test z D ¡0:54, p D 0:6; ® 0 D 0:025).

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TABLE 1. Dominance hierarchy of the black-and-white colobus females ID

Age classa

IBI

Dominant individual

(age in years) Ta Ma Ka Ir Sa Mo Mi Tu Ky Total

A A A A A S/A (7) SA (6) SA (3.5) SA (6)

32 24 –b 22 26

Submissive individual Ta

Ma

Ka

¤

4

1

1

¤

2

Total

Ir

Sa

Mo

Mi

Tu

Ky

¤

4 2 2 2

5

3 2

3

1

¤

8 10 3 3 6 3

1 1 2 4 3 2 4

1

1

1 2

¤

3 5 1 5 6 2 5 2

1

¤

26 22 10 17 21 7 12 3 5

11

11

36

18

29

123

¤

¤

1

1

6

5

1 2 5

6

¤

‘ID’ D identity of individuals; ‘IBI’ D interbirth interval between two infants that survived past 1 year of age; Age classes: A D adult, S/A D physically possibly adult, no sexual behaviour, SA D sub-adult, no sexual behaviour, smaller than adult females. a Estimated age in years at end of 1997 in brackets, estimations based on weaning situation in July 1992 when observations on the group started and July 1995 when Tu (possibly immigrated with mother) was Ž rst mentioned. b After Ky no infant of Ka survived past the age of one year.

Females groomed other females more often than they groomed the male, 0.97 and 0.046 interactions per focal observation hour respectively (in 1275 focal observation hours). Statistical tests could only be performed with the ad libitum data on grooming interactions. These data revealed that females in general groomed another female signiŽ cantly more often than the male (uncorrected values: Wilcoxon matched pairs signed ranks test z D ¡2:68, p D 0:0074). However, this apparent preference disappeared after correction for group composition (corrected values: Wilcoxon matched pairs signed ranks test z D ¡0:2, p D 0:86; ® 0 D 0:025). A comparison between red and black-and-white colobus females Fruits are generally assumed to evoke more contest competition than leaves or  owers. No difference was found between the species in the percentage of leaves in their diet (Wilcoxon matched pairs tests paired per month for 16 months: z D ¡0:57, p D 0:57), but red colobus fed less on fruits (N D 16 months, z D ¡2:07, p D 0:039) and more on  owers (N D 12 months, z D ¡2:7, p D 0:006) than black-and-white colobus. The size of

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food trees is generally assumed to determine inter-group competition: larger trees are expected to be more often contested than small trees. Red colobus foraged in larger trees than did black-and-white colobus (3951 and 1878 trees for Bad2A and Pol1 respectively, Mann-Whitney U -tests: z D ¡8:1, p D 0:000). Food that can be consumed readily is expected to be less contestable than food that requires a long handling time per item. Red colobus picked more food items per minute than did black-and-white colobus (N D 60 and 63 respectively; Mann-Whitney U -tests: z D ¡2:9, p D 0:003). Foraging red colobus females moved between food spots within trees or lianas more often than did foraging black-and-white colobus females (Fig. 2; Kaplan Meier test, loglinear, statistic D 5:5, df D 1, p D 0:0195). Measuring food spot residence time at the level of entire trees or patches of similar trees, instead of within a tree as done above, was very difŽ cult for red colobus groups, which forage over a wide stretch of forest and for which groups are very large. Therefore, as an indirect measurement of food spot residency time of a group, we measured the general use of space. We measured the distances that the group moved per hour and calculated the coefŽ cient of variation (variance/mean) in these distances for each day. Daily coefŽ cients of variation were higher for the black-and-white colobus group than for the red colobus group (Mann-Whitney U -test NRC D 190, NBWC D 309, z D ¡3:46, p D 0:001). The red colobus group apparently moved through the forest at a steady pace in comparison to the ‘stop-and-go’ manner of the black-and-white colobus group. This is not surprising, knowing that both species use trees of comparable sizes and a red colobus group, which is 4-5 times the size of a black-and-white colobus group, will deplete a tree of a given size much faster than a black-and-white colobus group. Agonistic interactions among females seemed less common in the red colobus group than in the black-and-white colobus group (data-sets too small for statistical analyses). Red colobus females were more likely to have a neighbour than black-and-white colobus females (Fig. 3; uncorrected percentages N D 15 and N D 6 females respectively; MW U D 9, z D ¡2; 8, p D 0:005), but females of both species were equally likely to have a female neighbour (Fig. 3; uncorrected percentages Mann-Whitney U D 38, z D ¡0:55, p D 0:59). Red colobus females groomed other individuals more frequently than did black-and-white colobus females (Fig. 4; uncorrected percentages Mann-Whitney U D 13, z D ¡2:78, p D 0:005). When we corrected for

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Fig. 2. Food spot residence time for red and black-and-white colobus depicted as the cumulative survival, ‘Cum Survival’, of each category of one minute time periods measured as the relative number of samples still continuing or being truncated at each one-minute interval. AC, for red colobus group Bad2A, or a diamond, for black-and-white colobus group Pol1, denotes that ‘censored’ (D truncated) data had ended. A low value of Cumulative Survival indicates that most samples had a shorter ‘Food spot residence time’ than the one at that speciŽ c time interval. Non-censored samples: NBad2A D 82, NPol1 D 59; truncated samples: NBad2A D 47, NPol1 D 53. Quartiles (25-50-75%) for Bad2A: non-censored samples: 1.0-1.0-2.0; censored samples: 1.0-3.0-5.0; for Pol1: Non-censored samples: 1.0-1.0-2.0; censored samples: 2.0-4.0-7.0.

group composition, red colobus females tended to groom males more than females and tended to seek the company of males above females while blackand-white colobus females showed no preference. The opposite was found for the uncorrected percentages (Fig. 3).

Discussion Relationships among eastern red colobus females have been described as egalitarian with strong bonds between males and females but weak bonds

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Fig. 3. The percentage of scans that females spent with any adult or sub-adult neighbour independent of sex, with an adult or sub-adult female (‘female’), and with an adult or sub-adult male (‘male’) for red (‘Bad2A’) and black-and-whitecolobus (‘Pol1’). The boxplots represent the quartiles and minimum and maximum values; ‘N’ D number of sampled females.

among females, and females are generally not involved in aggressive interactions with females of other groups (Struhsaker, 1975, 1980; Struhsaker & Oates, 1975; Struhsaker & Leland, 1979). Our results support these observations. The red colobus females living in Abuko (in a small forest patch), however, do become aggressive when they encounter females from other groups (Starin, 1991, 1994). In all populations of red colobus, females disperse from their natal group and males are philopatric despite an occasional solitary period during sub-adulthood (Struhsaker, 1975, 1980; Struhsaker & Oates, 1975; Struhsaker & Leland, 1979; Marsh, 1979a, b; Starin, 1991, 1994). Although we had little data on dispersal of females it seems unlikely that the red colobus of Taï differ in this respect. In comparison to red colobus, black-and-white colobus females were often involved in agonistic interactions with females of their own or of different groups. We could construct a linear dominance hierarchy among the black-

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Fig. 4. The percentage of focal minutes that females were grooming for red (‘Bad2A’) and black-and-white colobus (‘Pol1’) depicted as boxplots with minimum, maximum values and quartiles; ‘N ’ D number of sampled females.

and-white colobus females of a group, but the agonistic interactions in dyads of black-and-white colobus females were not uni-directional. Dominance rank was based on individual power and was not attained through the formation of alliances. In line with this relatively egalitarian dominance hierarchy, no effect of dominance rank on female reproductive success was evident. Females did not associate or groom preferentially with females. The results of this study differ slightly with results from other studies on the same or closely related species. In the Gambia C. polykomos females do not act aggressively toward females of other groups and they prefer to afŽ liate with females to males. In the closely related species (C. guereza) in at Kibale, Uganda, females are not involved in inter-group aggression and they afŽ liate preferentially with females compared to males (Oates, 1977; Struhsaker & Leland, 1979). In C. guereza at Kakamega, Kenya, females are occasionally involved in aggressive interactions with females from other groups, and aggressive interactions within the group are rare (Fashing, 2001a, b). Since the measures of afŽ liative interactions differ between observers, the most obvious difference between the black-and-white colobus in Taï and those at other sites is the competition between females of different groups. The difference between the red and the black-and-white colobus species of Taï and the difference among different populations of red

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or black-and-white colobus species indicate that phylogenetic inertia is not an important constraint on female involvement in inter-group con ict. If female social behaviour is adapted to their environment, females are expected to compete most strongly over high value food patches. Food was expected to be less contestable when handling time and food spot residence time were shorter. Indeed, in accordance with an apparently lower level of aggression among females, red colobus consumed food that required less handling time and more movements between foraging spots. Furthermore, in black-and-white colobus agonistic interactions tended to be most common over food items that required longer processing times. The importance of food spot residence time was not supported by the results on agonistic interactions in black-and-white colobus. The competition within a certain tree depends further on the number of individuals relative to the size of the tree. Red colobus foraged in slightly larger trees than did black-and-white colobus. Groups of red colobus, however, were also much larger than those of black-and-white colobus. It is therefore likely that the relatively lower level of intra-group aggression among red colobus females was a result of two factors which made food less easy to monopolise compared to that of black-and-white colobus: food patch size and selection for easy to process food items. Data on intra-group competition and details on food characteristics such as food spot residence time and handling time are limited and for a stronger test further investigation at the individual level is required. In relation to group size it seems reasonable to argue that food patches of black-and-white colobus were relatively large and therefore worth defending, while a similar tree would have relatively less value for a red colobus group. The red colobus group moved through the forest at a steadier pace than the black-and-white colobus group. This is another indication that food sources of black-and-white colobus may be worth monopolising especially since some of their food items require a long handling time, thus forcing them to remain in a spot relatively long. It seems therefore reasonable to assume that the difference between the species in aggression between females of the same and of different groups is a result of the differences in selected food. Female bonding and inter-group aggression In the socio-ecological models (see Isbell & Young, this volume) strong contest competition between females of different groups is closely linked

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to female philopatry and strong afŽ liative relationships among females. The data of the black-and-white colobus suggest otherwise: females did not spend more time grooming than red colobus females. What is more, black-andwhite colobus females were not strictly philopatric. Female dispersal in combination with female inter-group aggression is also found in muriquis (Strier et al., 1993), mantled howler monkeys (Glander, 1992), red howler monkeys (Pope, 2000), and red colobus in Abuko, the Gambia (Starin, 1991, 1994). The connection between dispersal system and inter-group food competition, therefore, may not be as strong as suggested by the theoretical formulations of the model. In fact, kinship is not a prerequisite for co-operation. It is most likely that kinship is less important when both (or all) coalition partners receive direct beneŽ ts from the joined effort (Harcourt, 1989). Thus, co-operation during inter-group con icts may result from the convergence of goals of unrelated individuals, a collective beneŽ t. Many examples exist of unrelated individuals that co-operate (e.g. baboons: Bercovitch, 1988; Noë, 1990; dolphins: Connor et al., 2001; ruffs: Hill, 1991; long-tailed manakin: McDonald & Potts, 1994; see further Pusey & Packer, 1997). Therefore, the assumption of the models that female intergroup competition necessarily leads to female philopatry may not be tenable. In conclusion, we can say that at least aggression among females of different groups is not constrained by phylogenetic inertia. Intra-group social relationships among females of red and black-and-white colobus differed only slightly and did not warrant refuting phylogenetic inertia as an important constraint. Female bonding, in the sense of philopatry, kin support, and afŽ liative interactions among females, appeared to be weak in both species, while inter-group aggression among females was pronounced in black-and-white colobus. This suggests that kin relations are not required for co-operative defense of food sources by groups of females against other groups. The differences between the species in food competition within and between groups could be linked to the value of food patches for females of the different species. Therefore, at least food competition among females seemed to re ect adaptations to food characteristics.

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