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View 33: 205–223 Primate super-groups? Polyspecific associations of captive monkeys A thesis submitted to the Miami University Honors Program in partial fulfillment of the requirements for University Honors with Distinction by Samantha Russak May 2006 Oxford, Ohio ii ABSTRACT PRIMATE SUPER-GROUPS? POLYSPECIFIC ASSOCIATIONS OF CAPTIVE MONKEYS By Samantha Russak Polyspecific (or heterospecific or mixed-species) groups are quite common among animals and vary greatly in their frequency, function, structure, and duration. The interactions between species may be very dynamic or passive with no apparent direct interactions. In the wild polyspecific groups are driven together by foraging and predation pressures; in captivity, mixed-species groups can be more stimulating for the animals. This paper examines three mixed-primate exhibits at the Lincoln Park Zoo over a 12-week period. One of these exhibits was fortuitously in the process of gaining a third species and so comparative data of before, during, and after stages were used for an in- depth analysis. Results show that some species, in this case howling monkeys, are little affected by the presence or absence of another species, while others, in this case sakis, are greatly impacted. iii iv Primate super-groups? Polyspecific associations of captive monkeys by Samantha Russak Approved by: _________________________, Advisor Dr. William C. McGrew _________________________, Reader Dr. Homayun Sidky _________________________, Reader Dr. Scott Suarez Accepted by: _________________________, Director, University Honors Program v vi ACKNOWLEDGEMENTS This project could not have been completed without the cooperation and assistance of the staff at Lincoln Park Zoo, particularly Dr. Sue Margulis, Andy Henderson, Bonnie Jacobs, Anita Yantz, Eric Meyers, and Leslie Lurz. I also thank Drs. William McGrew and Linda Marchant for their support and guidance throughout the project and Drs. Homayun Sidky and Scott Suarez for their help with the write-up of this manuscript. This research was funded by the Undergraduate Summer Scholars (USS) Program at Miami University, Ohio. vii TABLE OF CONTENTS List of Tables and Figures 9 Introduction 10 Methods Study Subjects 14 Data Collection 16 Results Solitary and Social Behaviors Titis, Goeldi’s monkeys, Allen’s swamp monkeys, guerezas 17 Howling monkeys 17 Sakis 18 Location Howling monkeys 19 Sakis 19 Discussion Solitary Behaviors and Social Interactions 20 Location 23 Implications and Future Studies 24 References 26 viii LIST OF TABLES AND FIGURES Tables Table 1. Ethogram 28 Table 2. Proximity data for two mixed-primate groups 29 Table 3. Partial behavioral repertoire of howling monkeys 29 Table 4. Location of howling monkeys within exhibit 30 Figures Figure 1. Partial behavioral repertoire of male saki 30 Figure 2. Partial behavioral repertoire of female saki 31 Figure 3. Partial behavioral repertoire of saki pair 32 Figure 4. Location of sakis within enclosure 33 ix - 10 - INTRODUCTION Large aggregations are not uncommon among animals, mostly being comprised of members of a single species. However, groups in which two or more species associate have also been well documented in both wild and captive settings. Polyspecific (or heterospecific or mixed-species) groups are best known in birds and mammals (Stensland et al., 2003), and among mammals, polyspecific associations in primates are perhaps the most studied (e.g. Chapman and Chapman, 2000). Such super-groups vary greatly in their frequency, function, structure, and duration, with species associating together for hours, days, weeks, or longer. The two main hypotheses as to why polyspecific associations occur are anti- predator and foraging advantages. Larger groups provide increased detection of both predators and food resources, and can more easily deter predators (through confusion or mobbing), displace smaller groups, or defend territory (Terbough, 1990; Waser, 1982). It has also been suggested that some species exploit the resource knowledge of their associates, with one species using another species as a “guide” to lead it to food resources (Norconk, 1990). Given these potentially important functions, it may be that polyspecific associations are co-evolved social structures, and if so, the consequent social relations may be important to participants. While the pressures of predation and foraging do not occur in zoos, there may be social benefits to housing together species that associate in nature. Captive mixed-species groups show greater overall activity levels and have richer (more stimulating) lives (Hardie et al., 2003). Most interspecific interactions in the wild are passive, with no apparent direct interactions. This includes tolerant spatial proximity resulting from a shared interest in - 11 - resources, such as food and habitat, as well as changes in behavioral patterns. For example, Chapman and Chapman (1996) found redtail monkeys to increase levels of vigilance when in association with another species. In a later study, Chapman and Chapman (2000) observed redtail monkeys to quickly follow red colobus groups when in association with this species; as black and white colobus rarely followed red colobus when in association, these findings suggest that redtail monkeys actively maintain their associations with red colobus, while black and white colobus simply tolerate the presence of red colobus. Dynamic interactions between species are much less common, and are usually limited to play among juveniles, such as in the case of white faced capuchins and mantled howling monkeys in Costa Rica (Rose et al., 2003) or contact aggression over food (e.g. Diana monkeys and putty-nosed monkeys during periods of low fruit availability; Eckardt & Zuberbühler, 2004). Similar interactions are observed among mixed-species groupings in captivity. However, as these groupings are predetermined by the facility’s staff, and as animals are spatially limited within enclosures, there is a greater risk for interspecific agonism or even violent encounters. This aggression can be overt, manifested in displacement, competition for space within an enclosure or food, or it can be subtle, evidenced as intimidation by social dominance or as stress (Thomas & Maruska, 1996). In contrast, species can be stimulated through non-hostile contact with one another. For example, Hardie et al. (2003) documented instances of interspecific playing and grooming within a tamarin mixed-species troop. - 12 - This paper presents an observational study of inter-species interactions between mixed-primate groups housed in three different exhibits at the Lincoln Park Zoo. These exhibits provided groupings reflecting different phylogenetic degrees of associations in the wild (either on a generic versus a specific level), therefore providing comparative data. Among New World primates, the most common participants of polyspecific associations (in the wild and captivity) are members of the subfamily Callitrichinae. For example, Goeldi’s monkeys (Callimico goeldii) are frequently found in association with tamarin (Saguinus) troops (Porter, 2001; Azevedo Lopes & Rehg, 2003). These associations are generally initiated by C. goeldii, and likely function to allow the parasitizing of Saguinus knowledge of fruit sources (Porter, 2001). Buchanan-Smith et al. (2000) found stable bispecific associations among tamarins in northern Bolivia, and occasionally observed trispecific associations with Callimico or Pithecia. This particular study included a mixed group of Callimico and Callicebus. Although geographical distributions of Goeldi’s monkey and members of the genus Callicebus (titi monkeys) commonly overlap, there is not much documented on associations between the two taxa. However, given that Goeldi’s monkeys and reed titi monkeys are within the same taxonomic family, and that Goeldi’s monkeys are often found in polyspecific associations, I hypothesized that this pairing would exhibit the most behaviors associated with affiliation, including play, social groom, and proximity as compared to the other two exhibits. Howling monkeys (Alouatta caraya) and sakis (Pithecia pithecia), are more closely related than the previous pair, and therefore might be expected to associate more - 13 - frequently. However, these two genera occupy very different dietary niches, with howlers being mainly folivorous and sakis being frugivorous, with a heavy reliance on seeds. This may explain observed occurrences of saki groups within proximity to howling monkeys with no apparent behavioral reactions (Vie et al., 2001). Further, it has been found that within a mixed-species group, the species with the larger body size tends to join the species with the smaller body size (Struhsaker, 1981). Therefore, with howlers being almost twice the size of sakis and the lack of direct interactions in the wild, I hypothesized that there would be fewer interactions than in the other two exhibits, and that most, if not all, of the associations that did occur would be initiated by the howlers. Among Old World primates, polyspecific associations are most commonly found among cercopithecines. In addition to associating with other cercopithecines, they are frequently found with colobines. Therefore, Colobus guereza and Allenopithecus nigroviridis are not an unlikely pairing. However, many studies (e.g. Chapman & Chapman, 1996; Struhsaker, 1981) have found Colobus to be the least frequent participant in polyspecific associations due to their shy and secretive nature. Further, Colobus spend most of their time in the
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