Primate Behavioral Ecology Research Articles

Gut microbiome is associated with personality traits of free-ranging Tibetan macaques (Macaca thibetana).

Recent studies have emphasized that there is a strong link between the gut microbiome and the brain that affects social behavior and personality in animals. However, the interface between personality and the gut microbiome in wild primates remains poorly understood. Here, we used high-throughput sequencing and ethological methods in primate behavioral ecology to investigate the relationship between gut microbiome and personality in Tibetan macaques (Macaca thibetana). The behavioral assessment results indicated three personality dimensions including socialization, shyness, and anxiety. There was significant variation in alpha diversity only for shyness, with a significantly lower alpha diversity indices (including Shannon, Chao1, and PD) for bold individuals than for shy individuals. Using regression models to control for possible confounding factors, we found that the relative abundance of three genera, Akkermansia, Dialister, and Asteroleplasma, was significantly and positively correlated with the sociability scores in the macaques. In addition, Oscillospiraceae exhibited a positive correlation with scores for Shy Dimension. Furthermore, we found that the predicted functional genes for propionate and pyruvate, porphyrin and chlorophyll metabolic pathways related to animal behavior, were significant enriched in shyness group. We propose that the gut microbiome may play an important role in the formation of personality of Tibetan macaques.

Effects of provisioning on the activity budget and foraging strategies of black-and-white snub-nosed monkeys (Rhinopithecus bieti) in the Baima Snow Mountain Nature Reserve, Yunnan, China.

Provisioning can significantly affect the ranging patterns, foraging strategies, and time budget of wild primates. In this study, we document for the first time, the effects of provisioning on the activity budget and foraging effort in an Asian colobine. Over 3-years, we used an instantaneous scanning method at 10-min intervals to collect data on the activity budget of a semiprovisioned breeding band (SPB) of black-and-white snub-nosed monkeys (Rhinopithecus bieti) (42-70 individuals) at Xiangguqing (Tacheng), Yunnan, China. We then compared the effects of provisioning in our study band with published data on a sympatric wild nonprovisioned breeding band (NPB) of R. bieti (ca. 360 monkeys) at the same field site. The SPB spent 25.6% of their daytime feeding, 17.1% traveling, 46.9% resting, and 10.3% socializing. In comparison, the NPB devoted more time to feeding (34.9%) and socializing (14.1%), less time to resting (31.3%), and was characterized by a greater foraging effort (1.74 versus 0.96, foraging effort = (feeding + traveling)/resting; see Methods). There was no difference between bands in the proportion of their activity budget devoted to traveling (15.7% vs. 17.1%). In addition, the SPB exhibited a more consistent activity budget and foraging effort across all seasons of the year compared to the NPB. These findings suggest that the distribution, availability, and productivity of naturally occurring feeding sites is a major determinant of the behavioral strategies and activity budget of R. bieti. Finally, a comparison of our results with data on six nonprovisioned R. bieti bands indicates that caution must be raised in meta-analyses or intraspecific comparisons of primate behavioral ecology that contain data generated from both provisioned and nonprovisioned groups.

Primates and pandemics: A biocultural approach to understanding disease transmission in human and nonhuman primates.

Investigations into zoonotic disease outbreaks have been largely epidemiological and microbiological, with the primary focus being one of disease control and management. Increasingly though, the human-animal interface has proven to be an important driver for the acquisition and transmission of pathogens in humans, and this requires syncretic bio-socio-cultural enquiries into the origins of disease emergence, for more efficacious interventions. A biocultural lens is imperative for the examination of primate-related zoonoses, for the human-primate interface is broad and multitudinous, involving both physical and indirect interactions that occur due to shared spaces and ecologies. I use the case example of a viral zoonotic epidemic that is currently endemic to India, the Kysanaur Forest Disease, to show how biocultural anthropology provides a broad and integrative perspective into infectious disease ecology and presents new insights into the determinants of disease outbreaks. Drawing on insights from epidemiology, political ecology, primate behavioral ecology and ethnoprimatology, this paper demonstrates how human-primate interactions and shared ecologies impact infectious disease spread between human and nonhuman primate groups.

Student research collaboration as conservation education: A case study from the primate field school at Maderas Rainforest Conservancy.

Maderas Rainforest Conservancy (MRC) is a conservation-focused non-profit organization that is devoted to protecting the tropical forests they manage in Costa Rica and Nicaragua and to providing conservation education for international university students through biological field schools. The MRC Primate Behavior and Ecology course is their most frequent course offering and is aimed at developing students to be independent field researchers. This course involves classroom lectures, training in primate identification and field methods, and the execution of independent research projects that students design, collect data for, and write up as scientific papers. Student development as conservationists is facilitated through the research experience provided by this field course as well as through co- and extracurricular research opportunities available to students at the sites that MRC manages: La Suerte Biological Research Station in Costa Rica, and Ometepe Biological Research Stationin Nicaragua. In tandem with their participation in the MRC primate field course, we (Laura M. Bolt and Amy L. Schreier) consistently offer students research opportunities in our ongoing project examining the impact of forest fragmentation on primate behavioral ecology. MRC student course evaluations indicate that this co- and extracurricular research participation substantially contributes to student academic development and conservation awareness. Student research collaboration, therefore, greatly benefits students as well as furthers MRC's conservation goals as a non-profit organization. In future MRC primate field school sessions, we will continue to offer research collaboration opportunities to students and will also endeavor to improve conservation education at MRC by involving more local community members in MRC's academic programs.

Fruit availability has a complex relationship with fission-fusion dynamics in spider monkeys.

Understanding the ecological and social factors that influence group size is a major focus of primate behavioural ecology. Studies of species with fission-fusion social organizations have offered an insightful tool for understanding ecological drivers of group size as associations change over short temporal and spatial scales. Here we investigated how the fission-fusion dynamics of spider monkeys (Ateles geoffroyi) at Runaway Creek, Belize were affected by fruit availability. When males and females were analyzed together, we found no association between fruit availability and subgroup size. However, when females were analyzed separately, we found that when fruit availability increased, so did subgroup size. In all analyses, higher fruit availability did not influence subgroup spatial cohesion. Our results point to the complexity of understanding grouping patterns, in that while ecological factors make groups of specific sizes advantageous, social factors also play an important determining role.

Primates got personality, too: Toward an integrative primatology of consistent individual differences in behavior.

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free-ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.

Investigating Niche Construction in Dynamic Human-Animal Landscapes: Bridging Ecological and Evolutionary Timescales

Human influence on the environment is evident at all landscape and ecological scales, from local to global, shaping both abiotic and biotic processes. Niche construction theory provides a means by which to investigate the consequences of these anthropogenic effects, but primatological research has been slow to integrate ecological and evolutionary timelines. We review methods that can be used to study how human niche construction influences nonhuman primates including phenological assessment, nonhuman primate behavioral observations, and ethnographic interview techniques. We argue that this approach provides a starting place to examine niche construction theory but that scholars of primate behavioral ecology must expand our methodologies to bridge the disconnect between ecological and evolutionary research time frames. We suggest areas of research and methods that have been underused but offer opportunities for integrative, innovative research. We conclude that an integrated, synthetic methodological approach is a major goal and that it will likely require a cross-disciplinary, collaborative effort.

Picturing Primates and Looking at Monkeys: Why 21st Century Primatology Needs Wittgenstein

AbstractThe Social Intelligence or Social Brain Hypothesis is an influential theory that aims to explain the evolution of brain size and cognitive complexity among the primates. This has shaped work in both primate behavioural ecology and comparative psychology in deep and far‐reaching ways. Yet, it not only perpetuates many of the conceptual confusions that have plagued psychology since its inception, but amplifies them, generating an overly intellectual view of what it means to be a competent and successful social primate. Here, I present an analysis of the Social Intelligence/Brain hypothesis highlighting how its anthropocentric origins have led us to be held captive by a picture of what social life involves and the kind of mind needed to navigate the social landscape. I go on to consider how experimental work in this vein either does not test what it claims to be testing, or introduces impossible problems regarding animal minds that cannot be solved, but only dissolved. What we need, in other words, is the application of “Wittgenstein's razor” and the reinvention of primatology along his enactivist lines.

Two Red-Capped Robin-Chats Cossypha Natalensis Imitate Antiphonal Duet of Black-Faced Rufous Warblers Bathmocercus rufus

ABSTRACT During my studies of primate behavioral ecology in the Kibale Forest, Uganda, I documented the first cases of red-capped robin-chats Cossypha natalensis imitating an antiphonal duet. In one case two individual robin chats imitated the entire duet of the black-faced rufous warbler Bathmocercus rufus, each giving both the male and female components. In a second case one robin chat gave the male components and another gave that of the female warbler. The lack of temporal separation between the male and female components of the warbler's antiphonal duet indicates an unusually high level of auditory perception and response time and cognitive ability on the part of redcapped robin-chats.

When the forest calls: My experience on the Primate Behavioural Ecology Field School in Cambodia

When the forest calls: My experience on the Primate Behavioural Ecology Field School in Cambodia

High dietary diversity supports large group size in Indo-Chinese gray langurs in Wuliangshan, Yunnan, China.

Identifying ecological factors underlying primate group size has been a central theme in primate behavioral ecology. The ecological constraints model proposes that increased group size leads to enhanced within-group feeding competition, necessitating increased travel to encounter additional or more productive feeding sites. Over the course of three years, we studied the largest known group (>80 individuals) of Trachypithecus crepusculus (Indo-Chinese gray langur) for 1738 hours during 213 days (including 96 full day follows) in Wuliangshan, China. During this period, group size increased from 81 individuals to over 90 individuals. The group consumed plant parts from 27 ± 8 (range: 15-51) species per month, and a total 148 plant species during the study. Based on time spent feeding, the diet was similar (54.2% leaves and 32.1% fruit and seeds) to that reported for other colobines. Despite occupying a home range several times larger than other groups of Trachypithecus, we found no evidence of an increase in daily path length with increasing group size, and the group's time budget and daily path length remained relatively constant despite marked monthly changes in dietary pattern (e.g. time spent exploiting fruit and seeds vs. buds and young leaves, vs. mature leaves). These results are inconsistent with many of the predictions of the ecological constraints model. Rather, our data suggest that high dietary diversity and the ability to exploit difficult to digest foods enabled Indo-Chinese gray langurs to reduce opportunities for feeding competition associated with increased group size.

Advances in Primate Community Ecology Research Across Spatial, Temporal, and Phylogenetic Scales

Understanding the factors influencing the diversity of primate communities is important for studies of primate evolutionary history, primate behavioral ecology, and the development of conservation strategies. Previous research on primate communities has focused on a variety of questions including explaining variation in species richness, biomass, and taxonomic composition (Kamilar and Beaudrot 2013; Reed and Bidner 2004), but with less attention given to the role of spatial scale in structuring communities, interactions between primates and other taxa, or evolutionary history. In recent years, there have been important advances in GIS, ecological informatics, macroecology, and phylogenetics, which have enabled scientists to revisit classic questions and address new questions in community ecology. This research has focused attention on the importance of variation in spatial, temporal, and phylogenetic scales for structuring communities (Beaudrot and Marshall 2011; Beaudrot et al. 2013; Gavilanez and Stevens 2013; Kamilar and Ledogar 2011; Kamilar and Muldoon 2010; Lehman 2006). The articles in this special issue of the International Journal of Primatology are based on a symposium at the 2013 American Association of Physical Anthropologists Meeting at Knoxville, Tennessee. The special issue includes a wide variety of perspectives to understand the diversity of primate communities across a variety of scales. The Int J Primatol (2014) 35:1083–1087 DOI 10.1007/s10764-014-9804-2

Activity Patterns, Intergroup Encounters, and Male Affiliation in Free-Ranging Bearded Sakis (Chiropotes sagulatus)

The assessment of how primates divide their daily activities is one of the foundations of primate behavioral ecology but the activity patterns and social behavior of the Pitheciines, including bearded sakis (genus Chiropotes), are poorly understood. During a 15-mo study, I collected 560 h of data on subgrouping, activity patterns, social behavior, and intergroup encounters of a group of free-ranging Guianan bearded sakis (Chiropotes sagulatus) in Guyana. The study group consisted of at least 65 individuals but showed a high degree of flexibility in grouping patterns (mean group size 39 ± 10). They were highly active, spending ca. 70% of their diurnal activity budget traveling and feeding. Activity patterns were relatively consistent throughout the year, although time spent feeding correlated significantly with fruit availability. The most common social behaviors were social resting and grooming. Agonism was rare (2.56% of social behavior) but did occur in the context of intergroup encounters, with males from the same group cooperating in intergroup agonism. Bearded sakis showed a high level of within group male affiliation, with male–male partners making up 65% of grooming dyads and males having another male as their nearest-neighbor 66% of the time. These results show that bearded sakis are characterized by egalitarian male–male and male–female relationships, highly fluid group sizes, and high levels of male affiliation. Similarities in the social behavior of bearded sakis and muriquis suggest several possible explanations for male–male bonding including cooperative defense of females from other groups, kinship, and maintenance of social cohesion after subgroup coalescence.

Contributions of sarah blaffer hrdy

Contributions of sarah blaffer hrdy

The Major Histocompatibility Complex and Primate Behavioral Ecology: New Tools and Future Questions

Since the serendipitous discovery of the effect of the major histocompatibility complex (MHC) on mate choice in laboratory mice nearly 40 yr ago, there has been sustained interest in the role that MHC genes may play in vertebrate sexual behavior. However, the challenges posed by MHC genotyping have long hampered progress in this area. We briefly introduce the documented links between MHC and behavior, before presenting an overview of the genotyping methods that were available before the introduction of new sequencing technologies. We then clarify why next-generation sequencing represents a major breakthrough in MHC genotyping by reviewing the recent successes —and pitfalls— of pioneer studies applying these techniques, before envisioning their revolutionary implications for future MHC studies in evolutionary ecology and primatology. We hope that our practical guidance to the design of MHC-based projects will promote and facilitate the integration of a MHC component into the research agendas of primatologists.

Major histocompatibility complex peptide ligands as olfactory cues in human body odour assessment

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Milinski Manfred, Croy Ilona, Hummel Thomas and Boehm Thomas 2013Major histocompatibility complex peptide ligands as olfactory cues in human body odour assessmentProc. R. Soc. B.2802013038120130381http://doi.org/10.1098/rspb.2013.0381SectionYou have accessCorrectionsMajor histocompatibility complex peptide ligands as olfactory cues in human body odour assessment Manfred Milinski Manfred Milinski Google Scholar Find this author on PubMed Search for more papers by this author , Ilona Croy Ilona Croy Google Scholar Find this author on PubMed Search for more papers by this author , Thomas Hummel Thomas Hummel Google Scholar Find this author on PubMed Search for more papers by this author and Thomas Boehm Thomas Boehm Google Scholar Find this author on PubMed Search for more papers by this author Manfred Milinski Manfred Milinski Google Scholar Find this author on PubMed Search for more papers by this author , Ilona Croy Ilona Croy Google Scholar Find this author on PubMed Search for more papers by this author , Thomas Hummel Thomas Hummel Google Scholar Find this author on PubMed Search for more papers by this author and Thomas Boehm Thomas Boehm Google Scholar Find this author on PubMed Search for more papers by this author Published:22 April 2013https://doi.org/10.1098/rspb.2013.0381This article corrects the followingResearch ArticleMajor histocompatibility complex peptide ligands as olfactory cues in human body odour assessmenthttps://doi.org/10.1098/rspb.2012.2889 Manfred Milinski, Ilona Croy, Thomas Hummel and Thomas Boehm volume 280issue 1755Proceedings of the Royal Society B: Biological Sciences22 March 2013Proc. R. Soc. B280, 20122889 (22 March 2013; Published online 23 January 2013) (doi:10.1098/rspb.2012.2889)In §2f, the final concentration of peptide solutions was incorrectly stated as 25 mM; it should read 25 µM. Previous ArticleNext Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Garamszegi L, Zagalska-Neubauer M, Canal D, Blázi G, Laczi M, Nagy G, Szöllősi E, Vaskuti É, Török J and Zsebők S (2018) MHC-mediated sexual selection on birdsong: Generic polymorphism, particular alleles and acoustic signals, Molecular Ecology, 10.1111/mec.14703, 27:11, (2620-2633), Online publication date: 1-Jun-2018. Leclaire S, Strandh M, Mardon J, Westerdahl H and Bonadonna F (2017) Odour-based discrimination of similarity at the major histocompatibility complex in birds, Proceedings of the Royal Society B: Biological Sciences, 284:1846, Online publication date: 11-Jan-2017. Natsch A (2017) Biochemistry and Genetics of Human Axilla Odor Springer Handbook of Odor, 10.1007/978-3-319-26932-0_49, (123-124), . Milinski M, Croy I, Hummel T and Boehm T (2014) Reply to A human chemo-sensory modality to detect peptides in the nose? by A. Natsch, Proceedings of the Royal Society B: Biological Sciences, 281:1776, Online publication date: 7-Feb-2014. Huchard E and Pechouskova E (2013) The Major Histocompatibility Complex and Primate Behavioral Ecology: New Tools and Future Questions, International Journal of Primatology, 10.1007/s10764-013-9700-1, 35:1, (11-31), Online publication date: 1-Feb-2014. Milinski M (2014) Arms races, ornaments and fragrant genes: The dilemma of mate choice in fishes, Neuroscience & Biobehavioral Reviews, 10.1016/j.neubiorev.2014.08.005, 46, (567-572), Online publication date: 1-Oct-2014. Related articlesMajor histocompatibility complex peptide ligands as olfactory cues in human body odour assessment22 March 2013Proceedings of the Royal Society B: Biological Sciences This Issue22 April 2013Volume 280Issue 1757 Article InformationDOI:https://doi.org/10.1098/rspb.2013.0381Published by:Royal SocietyOnline ISSN:1471-2954History: Published online22/04/2013Published in print22/04/2013 License:© 2013 The Author(s) Published by the Royal Society. All rights reserved. Citations and impact Large datasets are available through Proceedings B's partnership with Dryad

Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.

Do Nematode Infections of Red Colobus (Procolobus rufomitratus) and Black-and-White Colobus (Colobus guereza) on Humanized Forest Edges Differ from Those on Nonhumanized Forest Edges?

Forested edges, especially those that border humanized landscapes, provide opportunities for nonhuman primates and people to interact, and such interactions are predicted to alter disease dynamics. Given the rapid expansion of edge habitats globally, understanding changes occurring on edges is important in evaluating primate behavioral ecology and developing conservation plans. Our research investigates predictions concerning how gastrointestinal parasite and stress levels (cortisol) in red colobus and black-and-white colobus (Procolobus rufomitratus; Colobus guereza) in Kibale National Park, Uganda, differ between humanized and nonhumanized forest edges. We found Trichuris sp., an unidentified strongyle, and Strongyloides sp. in the fecal samples. Results did not generally support our expectation that humanized forest edges increase parasite infection and, counter to what we predicted, fecal cortisol did not differ between habitats, suggesting that proximity to edges and/or to humans did not result in increased stress. We conclude that broad habitat classifications, e.g., “humanized,” may be too general to identify consistent differences in parasite infection, as other factors, specific to the parasite (e.g., life cycled), host (e.g., immune systems strength), or environment (e.g., moisture level), likely also play important roles.

Predation and Predation Attempts on Red Titi Monkeys (Callicebus discolor) and Equatorial Sakis (Pithecia aequatorialis) in Amazonian Ecuador

Anecdotal reports of predation as well as observed predation attempts and rates of animal disappearance provide some of the most relevant data for evaluating the influence that predation risk may have on primate behavioural ecology. Here, we report rates of disappearance from six groups of red titi monkeys (Callicebus discolor) and two groups of equatorial sakis (Pithecia aequatorialis) followed over a period of four and a half years at a lowland site in Amazonian Ecuador. We also describe the first direct observation of a harpy eagle (Harpia harpyja) preying upon a titi monkey, as well as 3 unsuccessful attacks by tayras (Eira barbara) on titi monkeys and 4 unsuccessful attacks by various raptors on sakis. Our data indicate that pitheciid primates may face a wider array of possible predators than previously recognized, and that titi monkeys and sakis are susceptible to different major classes of predators. Our observations also suggest differences in the sex role during predator defence that could be related to the evolution and maintenance of monogamous systems.

A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang

Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost-effective alternative-the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring-tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally-derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high-frequency limits were comparable. However, at frequencies < or =2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10-dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR- and behaviorally-derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising technique for estimating primate hearing sensitivity, but that additional data are required to explore its efficacy for estimating low-frequency thresholds.