C 2004) International Journal of Primatology, Vol. 25, No. 6, December 2004 (
Interaction Between Capuchins and Coatis: Nonagonistic Behaviors and Lack of Predation ˆ de Resende,1,2 Massimo Mannu,1 Patr´ıcia Izar,1 Briseida Dogo and Eduardo B. Ottoni1 Received August 18, 2003; revision December 30, 2003; accepted January 29, 2004
We compare the nature of capuchin-coati interactions by Cebus apella in 2 populations under semifree-ranging and wild conditions. We report a similar pattern of interaction at both sites, in spite of their ecological differences. Most frequent capuchin behaviors toward coatis were agonistic, but we noted no predation. Contrarily, the monkeys also exhibited nonagonistic behaviors, such as play and grooming. As tufted capuchins predate other mammalian species, and as the subjects were aggressive towards competitor species, showing their belligerent temperament, we believe the lack of predation can be attributed to 2 different ecological contigencies – the absence of coati pups in a period of food shortage, and the cost of dealing with a dangerous adult coati where other rich resources were available–and also, perhaps, to different traditions in capuchin behavior towards coatis, established via intraspecific social learning. KEY WORDS: coati; capuchin; interspecific interactions.
INTRODUCTION Primate interspecific interactions may take a variety of forms depending on the nature of ecological relationships with different vertebrate species, especially as competitors, but also as mutualist, predators or prey. 1 Department
˜ Paulo, of Experimental Psychology, Institute of Psychology, University of Sao ˜ Paulo, SP, Brazil. Sao 2 To whom correspondence should be addressed at Avenue Professor Mello Moraes, 1721 – ˜ Paulo, SP, Brazil; e-mail:
[email protected]. CEP 05508-030, Sao 1213 C 2004 Springer Science+Business Media, Inc. 0164-0291/04/1200-1213/0
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Primates can interact aggressively with food competitors (Dias and Strier, 2000; Waser, 1997), predators (Boesch, 1994; Boinski, 1988; Chapman, 1986; Rose, 1997) and prey. Until recently, there were only a few reports of interspecific nonagonistic interactions, e.g., between bonobos and colobus monkeys and guenons (Ihobe, 1990, 1997; Sabater P´ı et al., 1993), and the capture and manipulation of hyraxes by chimpanzees, as if they were toys (Hirata et al., 2001), but no report came from systematic studies. Rose et al. (2003) presented a comparative study of interespecific interactions between Cebus capucinus and other species at 3 sites. The majority of interactions with competitors, predators, prey and neutral species were aggressive. However, they reported affiliative interactions between Cebus capucinus and 2 sympatric primate species, Alouatta and Ateles, in the form of play and grooming. Previously, considerable attention had been given to the predatory behavior of Cebus capucinus (Fedigan, 1990, Newcomer and De Farcy, 1985; Rose, 1997). Hunting vertebrates by primates is an infrequent behavior (Butynski, 1982) and there are only 2 species documented to prey systematically on vertebrates: the hunt of colobus, bush pigs or baboons by Pan troglodytes (Boesch, 1994; Goodall, 1990; McGrew, 1992) and the hunt of coatis (Nasua narica), birds and squirrels (Sciurus variegatoides) by Cebus capucinus (Newcomer and De Farcy, 1985; Perry and Rose, 1994; Rose, 1997). The apparent convergence between chimpanzees and capuchins in predatory behavior has led Rose (1997) to suggest that the tendency to behave aggressively towards other vertebrate species, including their own predators, might explain the evolution of their predatory behavior. Predation rates are variable across species and populations of Cebus (Rose, 1997; Rose et al., 2003). The higher number of predation reports for Cebus capucinus and C. olivaceus versus C. apella and C. albifrons could be an effect of different time of observation. Among Cebus capucinus, there is considerable interpopulational homogeneity in hunting behavior, but there are some differences regarding rates and killing techniques that could be at least partly attributed to social learning, but also to ecological differences (Perry et al., 2003). Tufted capuchins (Cebus apella) are omnivorous Neotropical primates that prey on several vertebrates: squirrels, other small mammals, frogs, lizards and birds (Ferreira et al., 2002; Galleti, 1990; Izawa, 1978; Resende et al., 2003; Terborgh, 1983). Nevertheless, in spite of the extensive overlap between the geographic range of the species and coatis (Nasua nasua: Emmons, 1997), wild tufted capuchin predation on coatis was never reported, even at sites where both species occur and where Cebus apella has been systematically studied (Di Bitteti, 1997; Izar, 1999; R´ımoli, 2001; Terborgh, 1983). We recorded no predation on coatis at our study sites. We report the nature of capuchin-coati interactions by 2 groups of Cebus
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apella, analyzing the features of this interaction that could explain the absence of coati predation. METHODS Subjects and Study Area Tietˆe Ecological Park (PET) We studied (since 1996) one semifree-ranging group (not constrained by physical barriers) of tufted capuchins in a reforested area of 180,000 m2 ˜ Paulo, Brazil (Ottoni and Mannu, 2001). at Tieteˆ Ecological Park, Sao Group size has varied from 15 to 26 individuals (Table I). The area is inhabited by several groups of coatis (Nasua nasua), at a density much higher than that observed for wild populations (Souza and Beisiegel, 2002). Adult male coatis are commonly among coati groups during the whole year, not only during the reproductive season—the usual pattern for the species (Martini and Beisiegel, 2002). Monkeys and coatis concentrate their activities around the same feeding area, resulting in daily encounters between the 2 populations. Tufted capuchins and coatis have dietary overlap, foraging on naturally available food items such as fruits and invertebrates, and on daily provisioned food (fruits and chow) distributed on fixed platforms. We have no means to determine which proportion of the diet is obtained through provisioning or foraging; however, monkeys enjoy eating meat when available, preying on birds and small mammals, viz., rats and opossums, or even stealing meat from the park kitchen (Ferreira et al., 2002; Resende et al., 2003), which suggests that lack of hunger due to provisioning cannot adequately explain the absence of predation on coati pups. Carlos Botelho State Park (PECB) The Carlos Botelho State Park (PECB) is located in southeast˜ Paulo State (24◦ 00 to 24◦ 15 S, 47◦ 45 to 48◦ 10 W), ern Brazil, in Sao Table I. Group composition during most of 1996 to 2002 mo Subjects AM AF JM JF I
1999
2000
2001
2002
10 4 3 2 1
8 4 6 2 3
8 3 6 3 3
6 5 3 0 2
Note. A: Adult or Subadult; J: Juvenile; I: Infant; M: Male; F: Female.
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comprising an area of about 380 km2 within the Atlantic forest domain. The area is covered mainly by undisturbed forest (Dias et al., 1995). Tufted capuchins and coatis are not abundant: 1.5 and 0.7 sights per 10 km, respectively (Izar, unpub. data). Capuchins forage mainly on pulp of mature fruits, invertebrates and foliar base of bromeliads (Izar, 2004). Vertebrate predation is rare and has been observed only on frogs, during periods of fruit scarcity (Izar, unpub. data). Coatis also forage for pulp of mature fruits and invertebrates (Izar, pers. obs.)
Data Collection and Analysis PET We compiled data from 2 studies conducted in the PET that were primarily on nutcracking behavior and, therefore, not specifically designed to investigate monkey/coati interactions. The first study was conducted from January to December 1999 and the second from January 2000 to June 2002. Coatis nest in November/December, thus we registered 3 birth seasons during our data collection. We followed the capuchins from 2 to 5 days a week, and interactions between them and coatis were registered via 2 procedures: all occurrences sampling and focal—animal sampling (Martin and Bateson, 1993), totaling 1520 h of all-occurrences sampling and 585 h of focal— animal sampling. The categories of observed interactions are described on Table II. During focal sampling, only the focal subject was considered when more than one monkey was involved in the interaction. We used all-occurrences sampling to describe nest attacks and exploration/play events. We used focal-animal sampling scores to calculate a rate for interaction and a rate for each behavioral category: total scores/total h of observation. To calculate the age/sex rate, we summed up each individual’s rate and divided it by the number of subjects in each category (AM: Adult/Subadult Male; AF: Adult Female; JM: Juvenile Male; JF: Juvenile Female; I: Infant). Then, via BioEstat 2.0 software (Ayres et al., 2000), we applied Kruskal-Wallis tests to check the distribution of the behavior categories among age/sex categories, testing which pairs of classes were responsible for significance (Siegel and Castellan, 1988). When subject appeared in more than one age category because of its developmental age, we considered only the scores in the category to which it belonged most of the time in order to avoid violating the independence assumption of the test. When >1 monkey was involved in the interaction, we considered only the focal subject.
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Table II. Ethogram of observed interactions between monkeys and coatis Category Attack/Threat Play/Exploration
Grooming
Definition Monkey show their teeth to the target, with piloerection. They may move to and fro and side-to-side, and/or chase/push/bite the target. Monkeys, with play face (relaxed mouth and stretched lips) and in a play context, interact with coatis in a rough-and-tumble way: rolling on the ground and pulling coati’s fur. They can also leap in front of the target and give soft bites, pull/push/poke/tap or chase the target without piloerection. The lack of piloerection differentiates it from Attack/Threat. There were events in which monkeys examined coatis as they did with other elements of their environment. Explore, in some cases, looked like monkey object play and, on other occasions, social play among monkeys was registered soon after or just before the interaction with coatis. Monkeys clean coati’s fur of parasites, searching with their fingers or mouth.
PECB We collected data systematically for one group (Orange), from November 2001 to December 2002, totaling 1032 h of observation (Izar, 2004). We observed coatis pups inside Orange’s home range on December, and registered 2 birth seasons during our data collection. We followed Orange daily from dawn to dusk, from 5 to 20 days per mo. We registered all-occurrences of encounters between capuchins and coatis, including the behavior of both species, context and duration. Due to visibility restrictions in PECB, we did not record the identities of the capuchins and used the data only to analyze rates of encounters and the nature of interactions between the species. At PECB, we recorded encounters even when there was no interaction between the species, but not at PET, because coatis and monkeys were always together during much of the day. RESULTS PET Rates of Interaction Considering only focal-animal sampling data, monkeys interacted with coatis every 2.5 h, or 40 times per 100 h. According to data in Table III, Attack/Threat is by far the most frequent category of interaction when all age/sex classes are considered, while Grooming is the least frequent, being performed only by adults and
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Table III. Focal-animal sampling hours, number of subjects in each age/sex category, rates and frequency of interactions among capuchins and coatis Interaction
Attack/Threat Explorations/Play
Foc. (h)a N subjectb Rate Events Rate Events Rate AM AF JM JF I
129 62 182 79 124
10 4 6 3 5
0.68 0.49 0.31 0.66 0.13
82 30 43 26 13
0.62 0.49 0.24 0.62 0.04
77 30 30 24 5
Events
0.01 0 0.07 0.04 0.08
1 0 13 2 8
Grooming Rate Events 0.05 0 0 0 0
4 0 0 0 0
Note. A: Adult or Subadult; J: Juvenile; I: Infant; M: Male; F: Female. a Foc. = total hours of Focal-animal sampling. bN Subject = total number of subjects per class.
subadults per focal-animal sampling, but twice juvenile monkeys groomed coatis during all-occurrences sampling. Adults and subadults interacted with coatis more frequently than juveniles and infants did when all kinds of interactions are taken into account, but the opposite is true when we considered only Exploration/Play.
Attack/Threat and Exploration/Play Attack/Threat is unevenly distributed through age/sex classes (H = 113376, df = 4, p = 0.023) and tests post hoc revealed that adult males, adult females and juvenile females attacked and threatened coatis significantly more than infants did (Mean Rank: RAM = 17.9; RAF = 16.75; RJM = 11.33; RJF = 17; RI = 3.2; p AMI < 0.005; p AFI < 0.05; p JFI < 0.05). There is no significant difference between the rates of Attack/Threat performed by juvenile males and the other age-sex classes. When we consider only age classes, Attack/Threat is also unevenly distributed (H = 102582, df = 2, p < 0.01) and adults and juveniles attacked and threatened more than infants did (Mean Rank: RA = 17.57; RJ = 13.22; RI = 3.25; p AI = 0.005; p JI < 0.05). Exploration/Play was performed differently by the age-sex classes (H = 110489, df = 4, p < 0.05): Adult males and adult females explored and played less than juvenile males and infants did (Mean Rank: RAM = 9.65; RAF = 8.5; RJM = 19.41; RJF = 15.5; RI = 21.12; p AMJM < 0.05; p AMI < 0.05; p AFJM < 0.05; p AFI < 0.05). There is no significant difference between rates of Exploration/Play performed by juvenile females and the other age-sex classes. When only age classes are considered, Exploration/Play is also unevenly distributed (H = 105019, df = 2, p < 0.01): Adults explored and played less than juveniles and infants did (Mean Rank: RA = 9.32; RJ = 18.11; RI = 21.12; p AI < 0.01; p AJ < 0.01).
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Juveniles behaved like adults during Attacks/Threats, and like infants during Exploration/Play. Juvenile males behaved in an infant-like way when we considered Exploration/Play and juvenile females behaved in an adult-like way when we considered Attack/Threat. Accordingly, it seems that females mature earlier than males. Play Interactions From a total of 62 events of Exploration/Play registered through alloccurrences and focal sampling, 26 events could clearly be identified as play behavior, because monkeys exhibited the play face. Immature monkeys played with adult and young coatis. Coati response was registered in 14 play events: twice they tried to escape; twice they showed no reaction; and in 10, they responded positively to play. Among latter, 8 involved young coatis and one, an adult coati (in the remaining event, coati’s age was not registered). Three events were initiated by immature coatis, and the monkeys started the remainder. Nest Attacks During the all-occurrences sampling, we registered 4 cases of attack on different coatis nests by capuchins, which lasted 10–25 min. They occurred on Nov/3rd/2000, on Nov/11th/2000, on Nov/16th/2001 and on Jan/29th/2002. The episodes are not in Table III because they were difficult to classify. We did not register them as Exploration/Play because monkeys, that were excited and had piloerection did not exhibit the play face. Furthermore it was a tense situation in which capuchins were wary about adult defender coatis. Because they showed no clear agonistic behavior, the events are not included in Attack/Threat. In all of them, we observed that: 1) ≥2 immature capuchins were involved. In 3 cases, the remainder of the group foraged nearby. In one case, the dominant male and one subadult male from the capuchin group participated, but only threatening the defender adult coati. 2) ≥1 a monkey grabbed a coati pup. The monkeys carried 1–2 coati nestlings out of the nest, but let them fall (all 8 times): 3 times, the monkeys recovered the nestlings pups (twice during the first event, once during the second), 3 times they abandoned them (first, third and fourth events), and in the 2 remaining events an adult coati, probably the mother, rescued the pups (second event). The adult
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coati protected the nest, threatening the monkeys and recovering the dropped pups. 3) the monkeys left the place, following the group. The young monkeys were excited, with piloerection, but it did not look like a threat display. Contrarily, the adult coatis, threatened and attacked the monkeys. On 3 occasions, we were able to examine the dropped pups. Except for one, which was dead and ripped around the belly, they were alive but had injured tails, as if bitten. A juvenile ate something while holding the dead nestling. We could not tell if it was coati flesh, but the body seemed intact, except for the rip and the bite on the tail. The monkeys were not able to hold coatis for more than a few sec, except once, when a juvenile male examined the coati. He smelled and bit the nestling, rubbed and banged it against a tree trunk, in a way that recalled object manipulation patterns. PECB There were 0.85 encounters between capuchins and coatis in 100 h at PECB (n = 9). Among them, 8 were at feeding fruit trees: coati and monkey groups fed on the same tree without interaction 4 times (though coatis vocalized alarm calls), and monkeys threatened coatis 4 times (coatis escaped twice, and stepped back twice and once 2 juvenile capuchins played around an adult female coati, pulling and touching her, but she did not react). In only one encounter, not in a fruit tree, a coati group repelled a late juvenile monkey. Therefore, when capuchins and coatis interacted in PECB, the most common pattern was Attack/Threat from capuchins towards coatis. DISCUSSION Two major issues emerge from our data. First, in spite of differences in ecological conditions and in the rates of interaction between tufted capuchins and coatis in PET and PECB, the observed patterns of interaction were similar, with Attack/Threat representing the most common behavior exhibited by capuchins towards coatis, and nonagonistic interactions, such as play, occurring in lower frequencies and being mainly performed by immature individuals. The pattern can be a consequence of a predisposition of Cebus apella to behave aggressively towards competitor species and also a consequence of their tendency to explore and to play with other elements of environment, which could include other species, as Rose et al. (2003) suggested for Cebus capucinus. This suggestion is strengthened by the fact that, at PET, the influence of age on monkey interactions towards coatis
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mirrored intraspecfic interactions because immature individuals explored and played more than adults/subadults, which were more aggressive than Infants and Juveniles. The pattern of juvenile interactions differed between males, which played and explored as Infants did, and females, which threatened and attacked as adults/subadults did, which is in accordance with the fact that females mature earlier than males do (Harvey et al., 1987). Second, the pattern of interaction of Cebus apella with coatis observed differs from the observed for C. capucinus in Costa Rica, where they prey on coatis and do not exhibit affiliative interactions with them. Lack of predation on coatis by PET groups is not necessarily a typical pattern of Cebus apella because it can be related to the ecological conditions of the study sites: at PET, there is no food deficit, so the cost of dealing with an aggressive adult coati defending its nest (Rose et al., 2003) may not outweigh the benefits of getting meat, specially because they do obtain it from other sources, such as invertebrates, small mammals and birds (Ferreira et al., 2002; Resende et al., 2003). At PECB, food shortage occurs during the dry season (Izar, 2004) and coatis give birth in the wet season (Izar, pers. obs.); therefore, no coati pup is available when they would be a key resource, considering that they would only hunt pups. However, as rate of encounters between the species is low, we cannot rule out the possibility that they will eventually hunt coatis. We predict that coati predation by Cebus apella could occur under certain ecological conditions, such as food shortage for monkeys coinciding with coati birth season, high population density or high home range overlapping or both. Our prediction relies on the hypothesis of Rose et al. that coati predation by Cebus capucinus is related not only to ecological conditions but also to the belligerent temperament of the species (Rose, 1997; Rose et al., 2003). The reaction of Cebus apella to competitors such as howlers and muriquis at PECB, and howlers at PET, indicates that they are potentially as belligerent as Cebus capucinus are: in 6 registered encounters with howlers at PECB, capuchins attacked and threatened twice, and did not react in 4 times, and in 36 registered encounters with muriquis, capuchins attacked and threatened 19 times and 17 times there was no reaction (Izar, unpub. data). At PET, capuchins attacked and threatened howlers in 6 of 9 encounters, and thrice, there was no reaction (Resende, unpub. data). The coatis nest attacks by tufted capuchins at PET also suggest that huntings of coati pups could eventually occur there because they are strikingly similar to descriptions of coati nest raids by Cebus capucinus (Rose et al., 2003). However, at PET nest attacks were mainly performed by juveniles, in contrast with nest raids performed by white-faced capuchins, in which adults are the main hunters. In this respect, nest attacks at PET are somewhat similar to Exploration/Play because curiosity might be guiding
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the monkeys to inspect and to take coati offspring from the nest, like chimpanzees toying with hyraxes (Hirata et al., 2001). Another difference between Cebus apella and C. capucinus emerging from our data is the occurrence of affiliative interactions with coatis. It cannot be attributed to temperamental differences between species because C. capucinus exhibit affiliative interactions with competitor species, such as play and grooming with howler and spider monkeys (Rose et al., 2003). It is possible, then, that capuchins show one pattern of interaction towards competitor species, which can even include affiliation, and another pattern towards potential prey. We cannot exclude the role of the other interacting species towards monkeys in shaping the pattern. In an area where coatis are hunted by capuchins, they probably avoid or fight the monkeys during encounters, thus not allowing the chance occurrence of play or grooming events that could contribute to the development of a history of affiliative interaction. For instance, monkeys at PET frequently tried to play with coatis, but we also registered episodes in which coatis initiated play bouts with the monkeys. Intraspecific social learning processes can also play a role in the consolidation of a given pattern of interspecific interactions, since particular ways of dealing with other species can be learned by observation of older conspecifics, paving the way to the establishment of different and perhaps mutually exclusive traditions in interspecific interactions. ACKNOWLEDGMENTS We thank the Tieteˆ Ecological Park, where we conducted our study and Carlos Eduardo Guidorizzi de Carvalho, who helped in the data collection. This work was supported by FAPESP (EBO: 97/14443, BDR: 99/11573-2, PI: 00/01052-4 and 00/14590-4), CNPq (EBO) and CAPES (MM) grants. We are very grateful for the extensive review provided by two anonymous reviewers. REFERENCES Ayres, M., Ayres, M. Jr., Ayres, L., and Santos, A. S. (2000). BioEstat 2.0: Aplicac¸oes ˜ ´ ´ Belem, ´ Estat´ısticas nas Areas de Ciˆencia Biologicas e M´edicas, Sociedade Civil Mamiraua. ´ Brazil. Boesch, C. (1994). Cooperative hunting in wild chimpanzees. Anim. Behav. 48: 653–667. Boinski, S. (1988). Use of a club by wild white-faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper). Am. J. Primatol. 54: 86–99. Butynski, T. M. (1982). Vertebrate predation by primates: A review of hunting patterns and prey. J. Hum. Evol. 11: 421–430.
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Resende, B. D., Greco, V. L. G., Ottoni, E. B., and Izar, P. (2003). Some observations on the predation of small mammals by tufted capuchin monkeys (Cebus apella). Neotrop. Primates. 11: 103–104. R´ımoli, J. (2001). Ecologia de macacos-prego (Cebus apella nigritus, Goldfuss, 1809) na Estac¸a˜ o Biologica de Caratinga (MG): implicac¸oes ´ ˜ para a conservac¸a˜ o de fragmentos de ´ Mata Atlˆantica, Unpublished Doctoral Thesis, Biological Sciences, University of Para, ´ Brazil. Belem, Rose, L. (1997). Vertebrate predation and food-sharing in Cebus and Pan. Int. J. Primatol. 18: 727–765. Rose, L., Perry, S., Panger, M., Jack, K., Manson, J., Gros-Luis, J., MacKinnon, K., and Vogel, W. (2003). Interspecific interactions between Cebus capucinus and other species: Data from three Costa Rican sites. Int. J. Primatol. 24: 759–796. Sabater P´ı, J., Bermejo, M., Illera, G., and Vea, J. J. (1993). Behavior of Bonobos (Pan paniscus) following their capture of monkeys in Zaire. Int. J. Primatol. 14: 797–804. Siegel, S., and Castellan, N. J. (1988). Nonparametric Statistics for the Behavioral Sciences, McGraw-Hill, Boston. Souza, A. P., and Beisiegel, B. M. (2002). O comportamento do quati, Nasua nasua, em situac¸a˜ o de alta densidade populacional. Anais do XX Encontro Anual de Etologia, Natal, Brazil, p. 304. Terborgh, J. (1983). Five New World Primates, Princeton University Press, Princeton, NJ. Waser, P. E. (1997). Interactions among primate species. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 210–226.
