Primate Field Studies Research Articles

Towards an integrated understanding of dietary phenotypes.

Diet and nutrition comprise a complex, multi-faceted interface between animal biology and food environments. With accumulating information on the many facets of this association arises a need for systems-based approaches that integrate dietary components and their links with ecology, feeding, post-ingestive processes and the functional and ecological consequences of these interactions. We briefly show how a modelling approach, nutritional geometry, has used the experimental control afforded in laboratory studies to begin to unravel these links. Laboratory studies, however, have limited ability to establish whether and how the feeding and physiological mechanisms interface with realistic ecological environments. We next provide an overview of observational field studies of free-ranging primates that have examined this, producing largely correlative data suggesting that similar feeding mechanisms operate in the wild as in the laboratory. Significant challenges remain, however, in establishing causal links between feeding, resource variation and physiological processes in the wild. We end with a more detailed account of two studies of temperate primates that have capitalized on the discrete variation provided by seasonal environments to strengthen causal inference in field studies and link patterns of intake to dynamics of nutrient processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Urinary cytokine measurements do not reflect surgery-induced inflammation in rhesus macaques.

Measurement of the health and disease status of free-ranging primates is often limited by a lack of available biomarkers of immune activation and inflammation that can be applied noninvasively via the measurement of urine or fecal samples. Here, we evaluate the potential usefulness of noninvasive urinary measurements of a number of cytokines, chemokines, and other markers of inflammation and infection. We took advantage of surgery-associated inflammation in seven captive rhesus macaques, collecting urine samples before and after the medical interventions. We measured these urine samples for 33 different markers of inflammation and immune activation that are known to be responsive to inflammation and infection in rhesus macaque blood samples, via the Luminex platform. We also measured all samples for concentrations of the soluble urokinase plasminogen activator receptor (suPAR),which we had validated in a prior study as an effective biomarker of inflammation. Despite urine samples being collected in captivity under ideal conditions (clean, no contamination with feces or soil, frozen quickly), 13/33 biomarkers measured via Luminex were found at concentrations below detection limits in >50% of samples. Of the remaining 20 markers, only 2 showed significant increases in response to surgery-IL18 and MPO (myeloperoxidase). However, suPAR measurements of the same samples show a consistent marked increase in response to surgery that is absent from the patterns of IL18 and MPO measurement. Given that our samples were collected under conditions that are greatly preferable to those usually encountered in the field, urinary cytokine measurements via the Luminex platform seem overall unpromising for primate field studies.

Insights into human evolution from 60 years of research on chimpanzees at Gombe.

Sixty years of research on chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania have revealed many similarities with human behaviour, including hunting, tool use, and coalitionary killing. The close phylogenetic relationship between chimpanzees and humans suggests that these traits were present in the last common ancestor of Pan and Homo (LCAPH). However, findings emerging from studies of our other closest living relative, the bonobo (Pan paniscus), indicate that either bonobos are derived in these respects, or the many similarities between chimpanzees and humans evolved convergently. In either case, field studies provide opportunities to test hypotheses for how and why our lineage has followed its peculiar path through the adaptive landscape. Evidence from primate field studies suggests that the hominin path depends on our heritage as apes: inefficient quadrupeds with grasping hands, orthograde posture, and digestive systems that require high quality foods. Key steps along this path include: (1) changes in diet; (2) increased use of tools; (3) bipedal gait; (4) multilevel societies; (5) collective foraging, including a sexual division of labor and extensive food transfers; and (6) language. Here I consider some possible explanations for these transitions, with an emphasis on contributions from Gombe.

Stability of chimpanzee (Pan troglodytes) urinary reproductive hormones during long-term preservation on filter paper.

Urine contains multiple water-soluble hormones, which are valuable non-invasive biomarkers for the monitoring of reproductive status and health. An effective method for drying urine on filter paper was previously developed to preserve wildlife urine samples where electrical equipment was not available for this; however, the stability of samples preserved in this way remains to be verified. Here, we developed and validated a method to elute multiple water-soluble reproductive hormones from filter paper that had been stored for an extended period of time. Aliquots of urine from chimpanzees were adsorbed on filter papers, air dried and stored for 1 year at room temperature. Estrone-3-conjugate (E1C), pregnanediol-3-glucuronide (PdG), estriol-3-glucuronide (E3G), and chorionic gonadotropin (CG) were eluted into deionized water from the filter papers and measured using enzyme immunoassays (EIAs). The mean recoveries of E1C, PdG, and creatinine from filter papers stored for 1year were 69.5%, 128.7%, and 83.8%, respectively. The profiles of E1C and PdG from preserved filter papers significantly correlated with those derived from a direct analysis of the frozen urine of menstruating chimpanzees. We detected E3G and CG from 1-year-old filter papers for urine collected during early pregnancy, but the recovery of E3G was low and CG profiles did not correlate with those of the original frozen urine samples. The method proposed here for the elution and measurement of reproductive hormones in urine preserved for a long period of time on filter paper provides a practical and simple way to monitor the reproductive status of chimpanzees. We propose that this method can also be utilized in field studies of other wild nonhuman primates.

Why Natural History Is Important to (Primate) Science: A Baboon Case Study

Natural history was the scientific approach used in early primate field studies and through the 1960s. After that, natural history fell out of favor, considered either bad science or not science at all. In my plenary talk at the 2018 IPS Congress in Nairobi, I argued that primate science once again needs natural history. Here, I reprise that argument, illustrating the long and tortuous route that took me to this conclusion. I use information on wild baboons (Papio anubis) from my 47-year field study in Kenya to support my claims. I then explain the historical and current reasons why science, including primate science, needs natural history, particularly in the Anthropocene.

Distinguished primatologist address-moving from advocacy to activism: Changing views of primate field research and conservation over the past 40 years.

Field studies of wild nonhuman primates have grown exponentially over the past 40 years and our knowledge of primate behavior, ecology, and social, and mating systems has expanded greatly. However, we are facing a major extinction crisis with some 60% of all primate species listed as threatened and more than 75% of species with declining populations. The primary factor driving primate population decline is human population increase, which over the past 50 years has resulted in the unsustainable conversion and degradation of natural landscapes for industrial agriculture, the production of nonagricultural commodities for international trade, pastureland for cattle, dam construction, fossil fuel exploration, mining, and the construction of road networks and infrastructure to support large urban centers. Recent ecological modeling predicts that by the end of the century, the four primate-richest countries in the world will lose 32-78% of their existing primate habitat to agricultural expansion, and nine of the top 15 primate-richest countries are expected to have 80-100% of their primate species extinct or threatened with extinction. If we are going to save the world's primates, the time to act is now! Not only should all primate field research include a strong conservation component, but in addition we must actively join with our professional societies, zoos and research facilities, universities, conservation organizations, concerned business leaders, global citizens, like-minded political leaders, and grassroots organizations to inform, demand and direct governments, multinational corporations, and international organizations to engage in transformational change to protect biodiversity and seek environmental justice against those entities that actively destroy our planet. As the chief academic discipline dedicated to the study of primates, we must organize and collectively move from being advocates for primate conservation to becoming activists for primate conservation. This is a call to action.

Methods for capturing wild squirrel monkeys in a floodplain forest: A comparison of two techniques and two species


 
 
 Field studies of primates often require the capture and marking of individuals in order to monitor behavior, health and population parameters. However, there have been few field studies in which squirrel monkeys (genus Saimiri) have been successfully captured. Here we report results obtained using two different trapping methods to capture Saimiri vanzolinii and S. cassiquiarensis in Central Amazonia, Brazil. We constructed 20 trapping stations, each one consisting of a platform containing a pair of Tomahawk traps, which were monitored by camera traps and baited with half a bunch of bananas, daily (at 6:00h and removed at 17:00h), during three months preceding the capture. We captured eight individuals of S. vanzolinii in two stations during five days (capture rate of 1.6 individuals/day). We were unable to capture individuals of S. cassiquiarensis using the Tomahawk traps; thus, we manually captured the individuals while they were foraging on the ground. To capture them, these individuals were first corralled and then captured with dip nets and leather gloves. We captured twelve individuals in seven days (capture rate of 1.7 individuals/day). We believe that both of these methods can be used for trapping squirrel monkeys, since they take into account the foraging strategies of the species, use of space, the presence of other competitive species such as capuchin monkeys, and the ecological features of the study area.
 
 

Geometry of nutrition in field studies: an illustration using wild primates.

Nutritional geometry has shown the benefits of viewing nutrition in a multidimensional context, in which foraging is viewed as a process of balancing the intake and use of multiple nutrients. New insights into nutrient regulation have been generated in studies performed in a laboratory context, where accurate measures of amounts (e.g. eaten, converted to body mass, excreted) can be made and analysed using amounts-based nutritional geometry. In most field situations, however, proportional compositions (e.g. of foods, diets, faeces) are the only measures readily available, and in some cases are more relevant to the problem at hand. For this reason, a complementary geometric method was recently introduced for analysing multi-dimensional data on proportional compositions in nutritional studies, called the right-angled mixture triangle (RMT). We use literature data from field studies of primates to demonstrate how the RMT can provide insight into a variety of important concepts in nutritional ecology. We first compare the compositions of foods, using as an example primate milks collected in both the wild and the laboratory. We next compare the diets of different species of primates from the same habitat and of the same species (mountain gorillas) from two distinct forests. Subsequently, we model the relationships between the composition of gorilla diets in these two habitats and the foods that comprise these diets, showing how such analyses can provide evidence for active nutrient-specific regulation in a field context. We provide a framework to relate concepts developed in laboratory studies with field-based studies of nutrition.

Lemur behaviour informs the evolution of social monogamy

Recent comparative analyses reached contradictory conclusions about the evolutionary origins of social monogamy in primates and other mammals, but they ignored variation in social bond quality between pair-partners. Recent field studies of Malagasy primates (lemurs) with variable intersexual bonds indicate independent evolutionary transitions to pair-living from solitary and group-living ancestors, respectively, as well as four cumulative steps in evolutionary transitions from a solitary life style to pair-living that resolve some contradictory results of previous studies.

The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra).

In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male (N = 4), adult female (N = 4), and juvenile (N = 5) wild black howler monkeys (Alouatta pigra) across a ten-month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host-microbe relationships in primate evolution.

Seasonal variation in the length of the daily activity period in buffy‐headed marmosets (Callithrix flaviceps): An important consideration for the analysis of foraging strategies in observational field studies of primates

Activity budgets are widely used in primate behavioral studies for the analysis of ecological strategies. In some cases, there is considerable seasonal variation in the length of the daily activity period. Here, activity budgets from two field studies of Callithrix flaviceps were compiled first by the traditional approach (proportion of scan sample records) and then by considering the proportion of time dedicated to each activity over the 24-hr cycle (adjusted budget). Both groups were almost invariably active for at least 1-2 hr less than the daylight period, with significantly shorter activity periods during the austral winter, when the daylight period was up to 2:35 hr shorter than in the summer. The adjustment of activity budgets provided a completely different perspective on foraging strategies. Whereas the basic budgets indicated a significant increase in foraging and moving during the resource-poor dry season (winter) months, the time-adjusted data revealed that the primary strategy was a time-minimizing one, with the animals simply spending more time at rest during the longer activity periods of summer days. While both groups followed the same pattern of relatively short activity periods, there were considerable differences between sites in the mean duration of the period in a given month, and in behavior patterns, although the analysis of the determining factors was beyond the scope of the present study. Overall, the results of the study indicate that the manipulation of the duration of the daily activity period may be an integral component of primate behavioral strategies, and that this parameter should be taken into account systematically when evaluating activity patterns, especially at sites at relatively high latitudes where day length may vary considerably over the course of the year.

Nutritional correlates of the “lean season”: Effects of seasonality and frugivory on the nutritional ecology of diademed sifakas

Primate field studies often identify "lean seasons," when preferred foods are scarce, and lower-quality, abundant foods (fallback foods) are consumed. Here, we quantify the nutritional implications of these terms for two diademed sifaka groups (Propithecus diadema) in Madagascar, using detailed feeding observations and chemical analyses of foods. In particular, we sought to understand 1) how macronutrient and energy intakes vary seasonally, including whether these intakes respond in similar or divergent ways; 2) how the amount of food ingested varies seasonally (including whether changes in amount eaten may compensate for altered food quality); and 3) correlations between these variables and the degree of frugivory. In the lean season, sifakas shifted to non-fruit foods (leaves and flowers), which tended to be high in protein while low in other macronutrients and energy, but the average composition of the most used foods in each season was similar. They also showed dramatic decreases in feeding time, food ingested, and consequently, daily intake of macronutrients and energy. The degree of frugivory in the daily diet was a strong positive predictor of feeding time, amount ingested and all macronutrient and energy intakes, though season had an independent effect. These results suggest that factors restricting how much food can be eaten (e.g., handling time, availability, or intrinsic characteristics like fiber and plant secondary metabolites) can be more important than the nutritional composition of foods themselves in determining nutritional outcomes-a finding with relevance for understanding seasonal changes in behavior, life history strategies, competitive regimes, and conservation planning.

Contributions of sarah blaffer hrdy

Contributions of sarah blaffer hrdy

Preface to the special contribution “Out of the tropics: ecology of temperate primates”

The distribution of most non-human primates falls largely into tropical regions, but some non-human primate taxa, e.g. some langurs, macaques, baboons, gibbons and lemurs, have successfully colonized temperate regions in East Asia, north and south Africa, Madagascar and South America (Fleagle 1999). Therefore, it is expected that these species exhibit a variety of adaptations that help them to cope with the ecological demands associated with living in marginal temperate habitats. Temperate-living primates are not necessarily less studied than tropical-living ones; for example, Japanese macaques have been studied at many study sites in the Japanese Archipelago for more than 60 years (Nakagawa et al. 2010), and their unique adaptations to coldness and strong seasonality, which are key characteristics of temperate habitats, have been well documented (Hori et al. 1977; Hanya 2004; Hanya et al. 2007). However, there have been few attempts to relate these findings to studies in tropical areas and to generalize the characteristics of temperate forests and the ecological strategies of primates that live there. The recent remarkable progress in primate field studies in continental temperate Asia, in particular China, now enables us to synthesize the compiled findings and obtain a better understanding of the general characteristics of temperate primates. For that purpose, we organized a symposium under the name of this special contribution at the XXIII Congress of the International Primatological Society in Kyoto on 16th September 2010. This special contribution is derived from the talks delivered at the symposium and complemented with additional papers. Five papers (Hanya et al. 2013; Sayers 2013; Grueter et al. 2013; Fan et al. 2013; Minhas et al. 2013) are included in the current issue, and more will follow in a subsequent one. We have included original case studies on the ecology of various temperate primates, such as macaques, colobines and gibbons. Each study examines how temperate-specific biotic and abiotic factors affect basic ecological adaptations, such as diet, activity budgets, ranging patterns and social organization. We have also included two papers that use a comparative approach and contrast temperate and tropical primates in terms of their habitat and diet, respectively. These papers amalgamate and integrate the current knowledge which until now has been scattered over the literature and present hypotheses that predict the sorts of adaptations that are required for primates to live and thrive in temperate forests. We believe that this special contribution marks a milestone in this interesting, yet-to-beexplored topic and will encourage further research on a more diverse range of taxa and in various geographic areas, thereby scrutinizing the validity of the ideas and hypotheses presented in our papers. We would like to thank all the contributors, editors and reviewers for their enthusiasm to make these important works available. The preparation of this special contribution was supported by the Kyoto University Foundation to Y.T. All the manuscripts were reviewed internally by the three of us before being submitted to the journal, after which they were reviewed in the same way as regular papers in this journal. G. Hanya (&) Y. Tsuji Primate Research Institute, Kyoto University, Kanrin 41-2, Inuyama, Aichi 484-8506, Japan e-mail: hanya@pri.kyoto-u.ac.jp

Peter M. Kappeler and David P. Watts (eds): Long-Term Field Studies of Primates

Peter M. Kappeler and David P. Watts (eds): Long-Term Field Studies of Primates

Technical note: Tree truthing: How accurate are substrate estimates in primate field studies?

Field studies of primate positional behavior typically rely on ground-level estimates of substrate size, angle, and canopy location. These estimates potentially influence the identification of positional modes by the observer recording behaviors. In this study we aim to test ground-level estimates against direct measurements of support angles, diameters, and canopy heights in trees at La Suerte Biological Research Station in Costa Rica. After reviewing methods that have been used by past researchers, we provide data collected within trees that are compared to estimates obtained from the ground. We climbed five trees and measured 20 supports. Four observers collected measurements of each support from different locations on the ground. Diameter estimates varied from the direct tree measures by 0-28 cm (Mean: 5.44 ± 4.55). Substrate angles varied by 1-55° (Mean: 14.76 ± 14.02). Height in the tree was best estimated using a clinometer as estimates with a two-meter reference placed by the tree varied by 3-11 meters (Mean: 5.31 ± 2.44). We determined that the best support size estimates were those generated relative to the size of the focal animal and divided into broader categories. Support angles were best estimated in 5° increments and then checked using a Haglöf clinometer in combination with a laser pointer. We conclude that three major factors should be addressed when estimating support features: observer error (e.g., experience and distance from the target), support deformity, and how support size and angle influence the positional mode selected by a primate individual. individual.

Long‐term field studies: positive impacts and unintended consequences

Long-term field studies of wild primates can have far-reaching impacts that transcend their contributions to science. These impacts can benefit not only the study animals, study areas, and local human communities, but they can also have unintended, potentially negative consequences. Examples of some of the positive impacts from the Northern Muriqui Project of Caratinga, in Minas Gerais, Brazil, include contributions to conservation efforts on behalf of this critically endangered species, capacity building through the training of Brazilian students, and employment opportunities for local people through our collaboration with a locally administered NGO that is facilitating ecotourism, education, and reforestation programs. Some concerns about unintended consequences of the research include the effects of our trails and trail traffic on surrounding vegetation and other aspects of the environmental "footprints" that both long-term researchers and short-term visitors may leave. In addition, although precautions against potential health risks from routine exposure to human observers are now standard protocol, little is known about the other ways in which our long-term research presence can affect the primates' experiences or alter their perceptions of their social and ecological environments. Risk analysis, which weighs both the positive and negative impacts can provide useful perspectives for addressing the ethical considerations that can arise during long-term field studies.

Ethics commentary: subjects of knowledge and control in field primatology

Our primate kin are routinely displaced from their habitats, hunted for meat, captured for trade, housed in zoos, made to perform for our entertainment, and used as subjects in biomedical testing. They are also the subjects of research inquiries by field primatologists. In this article, we place primate field studies on a continuum of human and alloprimate relationships as a heuristic device to explore the unifying ethical implications of such inter-relationships, as well as address specific ethical challenges arising from common research protocols "in the field" (e.g. risks associated with habituation, disease transmission, invasive collection of biological samples, etc.). Additionally, we question the widespread deployment of conservation- and/or local economic development-based justifications for field-based primatological pursuits. Informed by decades of combined fieldwork experience in Indonesia and the Democratic Republic of Congo, we demonstrate the process by which the adherence to a particular ethical calculus can lead to unregulated and ethically problematic research agendas. In conclusion, we offer several suggestions to consider in the establishment of a formalized code of ethics for field primatology.

Ethical issues faced by field primatologists: asking the relevant questions

Field primatologists face unusual ethical issues. We study animals rather than people and receive research approval from animal care rather than ethics committees. However, animal care evaluation forms are developed from concerns about laboratory animal research and are based on the "Three R's" for humane treatment of captive experimental subjects (replacement, reduction and refinement), which are only debatably relevant to field research. Scientists who study wild, free-ranging primates in host countries experience many ethical dilemmas seldom dealt with in animal care forms. This paper reviews the ethical issues many field primatologists say they face and how these might be better addressed by animal care forms. The ethical issues arising for field researchers are divided into three categories: "Presence, Protocols and People" and for each the most frequent issues are described. The most commonly mentioned ethical concern arising from our presence in the field is the possibility of disease transmission. Although most primate field studies employ only observational protocols, the practice of habituating our study animals to close human presence is an ethical concern for many since it can lessen the animals' fear of all humans, thereby facilitating undesirable behaviors (e.g., crop-raiding) and rendering them vulnerable to harm. Field primatologists who work in host countries must observe national laws and local traditions. As conservationists, primatologists must often negotiate between the resource needs and cultural practices of local people and the interests of the nonhuman primates. Many say they face more ethical dilemmas arising from human interactions than from research on the animals per se. This review concludes with suggestions for relevant questions to ask on animal care forms, and actions that field primatologists can take to better inform animal care committees about the common ethical issues we experience as well as how to develop guidelines for addressing them.

Long‐term field studies of primates: Considering the past, present, and future

Long‐term field studies of primates: Considering the past, present, and future