Mark Bowler

Diet and Food Choice in Peruvian Red Uakaris (Cacajao calvus ucayalii): Selective or Opportunistic Seed Predation?

Even primates considered dietary specialists tend to eat a combination of fruit pulp, seeds, other plant parts, or animals. Specialist seed predators could either feed on seeds preferentially, or to avoid competition when ripe pulps are scarce. Pitheciin monkeys have specialized dentition that allows them to feed on seeds protected by hard shells, and the upper limit on the hardness of these is likely to be a function of jaw size. We recorded the diet of Peruvian red uakaris (Cacajao calvus ucayalii) on the Yavari River, Peru, to test the prediction that this seed predator would feed on the seeds of hard-shelled fruits preferentially over softer ones in relation to their availability in the forest. We also tested predictions that adult male, adult female, and juvenile diets would differ, with larger individuals eating more hard fruits. Uakaris ate 55.4% seeds, 38.9% pulps and arils, and 5.6% other items, but proportions varied through the year. More pulps, especially from the palm Mauritia flexuosa, were eaten when fruit availability was low, and more hard fruits were positively selected for than softer ones. Juveniles did not open the hardest fruit species opened by adults, and adult males ate harder fruits than females. These results provide evidence that seed eating in some primates has evolved beyond a means of avoiding competition for the ripe pulps typically preferred by many primates. Specialist seeding-eating primates therefore occupy divergent niches that require separate consideration from those of similar-sized primates.

Evidence for Weak or Linear Conformity but Not for Hyper-Conformity in an Everyday Social Learning Context

Conformity is thought to be an important force in cultural evolution because it has the potential to stabilize cooperation in large groups, potentiate group selection and thus explain uniquely human behaviors. However, the effects of such conformity on cultural and biological evolution will depend much on the way individuals are influenced by the frequency of alternative behavioral options witnessed. Theoretical modeling has suggested that only what we refer to as ‘hyper-conformity’, an exaggerated tendency to perform the most frequent behavior witnessed in other individuals, is able to increase within-group homogeneity and between-group diversity, for instance. Empirically however, few experiments have addressed how the frequency of behavior witnessed affects behavior. Accordingly we performed an experiment to test for the presence of conformity in a natural situation with humans. Visitors to a Zoo exhibit were invited to write or draw answers to questions on A5 cards and potentially win a small prize. We manipulated the proportion of existing writings versus drawings visible to visitors and measured the proportion of written cards submitted. We found a strong and significant effect of the proportion of text displayed on the proportion of text in the answers, thus demonstrating social learning. We show that this effect is approximately linear, with potentially a small, weak-conformist component but no hyper-conformist one. The present experiment therefore provides evidence for linear conformity in humans in a very natural context.

Multilevel Societies in New World Primates? Flexibility May Characterize the Organization of Peruvian Red Uakaris (Cacajao calvus ucayalii)

Researchers have described multilevel societies with one-male, multifemale units (OMUs) forming within a larger group in several catarrhine species, but not in platyrhines. OMUs in multilevel societies are associated with extremely large group sizes, often with >100 individuals, and the only platyrhine genus that forms groups of this size is Cacajao. We review available evidence for multilevel organization and the formation of OMUs in groups of Cacajao, and test predictions for the frequency distribution patterns of male–male and male–female interindividual distances within groups of red-faced uakaris (Cacajao calvus ucayalii), comparing year-round data with those collected at the peak of the breeding season, when group cohesion may be more pronounced. Groups of Cacajao fission and fuse, forming subgroup sizes at frequencies consistent with an OMU organization. In Cacajao calvus ucayalii and Cacajao calvus calvus, bachelor groups are also observed, a characteristic of several catarrhine species that form OMUs. However, researchers have observed both multimale–multifemale groups and groups with a single male and multiple females in Cacajao calvus. The frequency distributions of interindividual distances for male–male and male–female dyads are consistent with an OMU-based organization, but alternative interpretations of these data are possible. The distribution of interindividual distances collected during the peak breeding season differed from those collected year-round, indicating seasonal changes in the spatial organization of Cacajao calvus ucayalii. We suggest a high degree of flexibility may characterize the social organization of Cacajao calvus ucayalii, which may form OMUs under certain conditions. Further studies with identifiable individuals, thus far not possible in Cacajao, are required to confirm the social organization.

Peruvian Red Uakari Monkeys (Cacajao Calvus Ucayalii) in the Pacaya-Samiria National Reserve — A Range Extension Across a Major River Barrier

2005. Foraging ecology of jaguar (Panthera onca) and puma (Puma concolor) in hunted and non-hunted sites within the Maya Biosphere Reserve, Guatemala.covery of a new sub-population of the black lion tama-rins (Leontopithecus chrysopygus) at Serra de Paranapia-caba, São Paulo, Brazil, Neotrop. Primates, 11(2): 75–76. Röhe, F. 2007. Mamíferos de médio e grande porte do médio Rio Madeira. (Puma yagouaroundi) food habits in mosaic of Atlantic Rainforest and eucalypt plantations of southeastern Brazil. Braz. Notas sobre félidos neotropicales VIII: Observaciones sobre el contenido estomacal y el compor-tamiento alimentar de diversas especies de felinos. Rev. According to Hershkovitz (1987) Cacajao calvus ucayalii, listed as Vulnerable by the IUCN, (Veiga & Bowler, 2008) is distributed from the east bank of the Rio Ucayali in an easterly direction to the Rio Yavarí and from the Rio Amazonas in the north to the Rio Urubamba in the south. Hershkovitz (1987) also includes the east bank of the lower Yavarí in Brazil, but its presence there has not been confirmed and it is possible that museum specimens marked as collected on the Brazilian bank of the Yavarí actually came from the Peruvian side where this primate is locally abundant. Surveys conducted between 1979 and 1986 (Aquino 1988) showed that the range was much reduced, hunting having exterminated the species in several areas. Aquino (1988) suggested that the southern limit is now probably the Rio Sheshea and that populations close to the Rios Ucayali and Amazonas have also been reduced and in some areas populations have been exterminated (Fig. 1). Populations of Cacajao calvus observed by Peres (1997) on the upper Rio Juruá and unconfirmed reports by Fernandes (1990) in the Brazilian state of Acre on the upper Juruá and Purus are either of Cacajao calvus novaesi or Cacajao calvus ucayalii, which would extend the known ranges of either of these subspecies. The Rio Ucayali is the largest tributary of the Rio Amazo-nas and at 400–1,200m wide presents a significant barrier to primate populations. However, the constantly-changing course of the river means that very large islands of forest

Assessing Public Engagement with Science in a University Primate Research Centre in a National Zoo

Recent years have seen increasing encouragement by research institutions and funding bodies for scientists to actively engage with the public, who ultimately finance their work. Animal behaviour as a discipline possesses several features, including its inherent accessibility and appeal to the public, that may help it occupy a particularly successful niche within these developments. It has also established a repertoire of quantitative behavioural methodologies that can be used to document the publics responses to engagement initiatives. This kind of assessment is becoming increasingly important considering the enormous effort now being put into public engagement projects, whose effects are more often assumed than demonstrated. Here we report our first attempts to quantify relevant aspects of the behaviour of a sample of the hundreds of thousands of visitors who pass through the ‘Living Links to Human Evolution Research Centre’ in Edinburgh Zoo. This University research centre actively encourages the public to view ongoing primate research and associated science engagement activities. Focal follows of visitors and scan sampling showed substantial ‘dwell times’ in the Centre by common zoo standards and the addition of new engagement elements in a second year was accompanied by significantly increased overall dwell times, tripling for the most committed two thirds of visitors. Larger groups of visitors were found to spend more time in the Centre than smaller ones. Viewing live, active science was the most effective activity, shown to be enhanced by novel presentations of carefully constructed explanatory materials. The findings emphasise the importance and potential of zoos as public engagement centres for the biological sciences.

Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia)

Neotropical monkeys of the genera Cacajao, Chiropotes, and Pithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a “local pattern” of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types. Am. J. Primatol. 74:1106‐1127, 2012.

Evolutionary Biology and Conservation of Titis, Sakis and Uacaris: Why we know so little: the challenges of fieldwork on the Pitheciids

Introduction Possessing a suite of unusual and interesting features, Pitheciids are at the extremes of many of primatology’s ecological and sociological continua (see Norconk 2011). Pitheciids should provide acute tests of many primatological models; however, this is frequently thwarted by the lack of even the most basic quantitative information concerning ecology, behavior and social organization. Such gaps are due not only to the small number of studies, but also to difficulties in obtaining data. This chapter considers why, given that these primates possess such aesthetic and intellectual appeal and high conservation value, they have been so little studied. The peculiarities of pitheciids, combined with their native habitats’ inherent challenges, have often undermined potentially successful fieldwork. Some researchers who began working with species of Callicebus or Chiropotes, for example, simply gave up because of problems habituating the animals or because the study was so difficult that the quality and quantity of gained data would not be worth the effort. Several researchers who persisted were either unable to obtain the expected volume of data or were incapable of answering many of their initial research questions, sometimes both. Using field experiences from a variety of research projects across a range of habitat types and pitheciid taxa, this chapter reports on the problems that arose during these studies and presents suggestions to minimize similar difficulties in the future.

Refining Reproductive Parameters for Modelling Sustainability and Extinction in Hunted Primate Populations in the Amazon

Primates are frequently hunted in Amazonia. Assessing the sustainability of hunting is essential to conservation planning. The most-used sustainability model, the ‘Production Model’, and more recent spatial models, rely on basic reproductive parameters for accuracy. These parameters are often crudely estimated. To date, parameters used for the Amazon’s most-hunted primate, the woolly monkey (Lagothrix spp.), come from captive populations in the 1960s, when captive births were rare. Furthermore, woolly monkeys have since been split into five species. We provide reproductive parameters calculated by examining the reproductive organs of female Poeppig’s woolly monkeys (Lagothrix poeppigii), collected by hunters as part of their normal subsistence activity. Production was 0.48–0.54 young per female per year, and an interbirth interval of 22.3 to 25.2 months, similar to parameters from captive populations. However, breeding was seasonal, which imposes limits on the maximum reproductive rate attainable. We recommend the use of spatial models over the Production Model, since they are less sensitive to error in estimated reproductive rates. Further refinements to reproductive parameters are needed for most primate taxa. Methods like ours verify the suitability of captive reproductive rates for sustainability analysis and population modelling for populations under differing conditions of hunting pressure and seasonality. Without such research, population modelling is based largely on guesswork.

Assessment of mammal reproduction for hunting sustainability through community-based sampling of species in the wild

Wildlife subsistence hunting is a major source of protein for tropical rural populations and a prominent conservation issue. The intrinsic rate of natural increase. (rmax ) of populations is a key reproductive parameter in the most used assessments of hunting sustainability. However, researchers face severe difficulties in obtaining reproductive data in the wild, so these assessments often rely on classic reproductive rates calculated mostly from studies of captive animals conducted 30 years ago. The result is a flaw in almost 50% of studies, which hampers management decision making. We conducted a 15-year study in the Amazon in which we used reproductive data from the genitalia of 950 hunted female mammals. Genitalia were collected by local hunters. We examined tissue from these samples to estimate birthrates for wild populations of the 10 most hunted mammals. We compared our estimates with classic measures and considered the utility of the use of rmax in sustainability assessments. For woolly monkey (Lagothrix poeppigii) and tapir (Tapirus terrestris), wild birthrates were similar to those from captive populations, whereas birthrates for other ungulates and lowland-paca (Cuniculus paca) were significantly lower than previous estimates. Conversely, for capuchin monkeys (Sapajus macrocephalus), agoutis (Dasyprocta sp.), and coatis (Nasua nasua), our calculated reproductive rates greatly exceeded often-used values. Researchers could keep applying classic measures compatible with our estimates, but for other species previous estimates of rmax may not be appropriate. We suggest that data from local studies be used to set hunting quotas. Our maximum rates of population growth in the wild correlated with body weight, which suggests that our method is consistent and reliable. Integration of this method into community-based wildlife management and the training of local hunters to record pregnancies in hunted animals could efficiently generate useful information of life histories of wild species and thus improve management of natural resources.

Mutual medication in capuchin monkeys - Social anointing improves coverage of topically applied anti-parasite medicines.

Wild and captive capuchin monkeys will anoint themselves with a range of strong smelling substances including millipedes, ants, limes and onions. Hypotheses for the function of the behaviour range from medicinal to social. However, capuchin monkeys may anoint in contact with other individuals, as well as individually. The function of social anointing has also been explained as either medicinal or to enhance social bonding. By manipulating the abundance of an anointing resource given to two groups of tufted capuchins, we tested predictions derived from the main hypotheses for the functions of anointing and in particular, social anointing. Monkeys engaged in individual and social anointing in similar proportions when resources were rare or common, and monkeys holding resources continued to join anointing groups, indicating that social anointing has functions beyond that of gaining access to resources. The distribution of individual and social anointing actions on the monkeys’ bodies supports a medicinal function for both individual and social anointing, that requires no additional social bonding hypotheses. Individual anointing targets hard-to-see body parts that are harder to groom, whilst social anointing targets hard-to-reach body parts. Social anointing in capuchins is a form of mutual medication that improves coverage of topically applied anti-parasite medicines.