Free-ranging Nonhuman Primates Research Articles

Non-invasive specimen collections for Mycobacterium tuberculosis detection in free-ranging long-tailed macaques (Macaca fascicularis).

Surveillance of infectious diseases in free-ranging or wild animals has been widely conducted in many habitat-range countries after the COVID-19 episode. Thailand is located in the center of the distribution range of long-tailed macaques (Macaca fascicularis; Mf) where the animals have both frequent human contact and a high prevalence of human tuberculosis. For the large-scale detection of Mycobacterium tuberculosis complex (MTBC) using IS6110-nested PCR in free-ranging Mf, non-invasive sampling was developed using oral (via rope bait) and fecal (direct swabs of fresh feces) specimen collection. Firstly, the MTBC-IS6110-nested PCR was validated in non-invasively collected specimens, in terms of its specificity and sensitivity, and then compared with those of the invasively collected oral and rectal swabs in 24 captive MTBC-suspected Mf. After validation, these methods were applied to survey for the prevalence of shed MTBC (MTBCS) in four previously reported MTBC-infected populations. A total of 173 baited rope specimens and 204 freshly defecated excretions were collected. The limit of detection of the IS6110-nested PCR technique was 10 fg/μL and the 181-bp PCR amplicon showed 100% sequence similarity with the MTB H37Rv genome sequence. Comparing the MTBCS detection between the invasive and non-invasive collected specimens in captive suspected Mf revealed a significant correlation between the two types of oral specimens (oral swabs and baited ropes; n = 24, r2 = 1, p-value < 0.001), but fresh fecal swabs showed higher MTBCS frequencies than the rectal swabs. Moreover, the proportion of MTBCS-positive free-ranging Mf were significantly higher in the fresh fecal swabs (8.82%; 95% CI; 4.9-12.7%) than in the baited ropes (5.20%; 95% CI; 1.9-8.5%). This result indicates that oral sampling via baited ropes and fecal sampling via defecated excretion swabs can serve as ancillary specimens for MTBCS detection in free-ranging non-human primates.

Hepato-pathological hallmarks for the surveillance of Yellow Fever in South American non-human primates

The early detection and diagnosis of deaths in free-ranging non-human primates (NHPs) are key points for the surveillance of Yellow Fever (YF) in Brazil. The histopathological identification of infectious diseases remains very useful and reliable in the screening and detection of emerging zoonotic diseases such as YF. We surveyed data records and liver slides stained with hematoxylin and eosin from the Epizootics Surveillance Network to control YF, Ministry of Health of Brazil, to evaluate histopathological hallmarks for the diagnosis of the YF virus infection. We selected natural fatal cases in NHPs from the genera Alouatta spp., Callithrix spp., and Sapajus spp. with a positive immunohistochemical assay for YF in liver samples. Our findings showed the full-spectrum YF-associated hepatic lesions in all NHPs, but some histopathological findings differed in the distribution and intensity between the three genera. In our study, South American NHPs showed significant differences in the YF-associated hepatic histopathological features compared to fatal cases reported in humans.

Fatal Human Alphaherpesvirus 1 Infection in Free-Ranging Black-Tufted Marmosets in Anthropized Environments, Brazil, 2012-2019.

Human alphaherpesvirus 1 (HuAHV1) causes fatal neurologic infections in captive New World primates. To determine risks for interspecies transmission, we examined data for 13 free-ranging, black-tufted marmosets (Callithrix penicillata) that died of HuAHV1 infection and had been in close contact with humans in anthropized areas in Brazil during 2012–2019. We evaluated pathologic changes in the marmosets, localized virus and antigen, and assessed epidemiologic features. The main clinical findings were neurologic signs, necrotizing meningoencephalitis, and ulcerative glossitis; 1 animal had necrotizing hepatitis. Transmission electron microscopy revealed intranuclear herpetic inclusions, and immunostaining revealed HuAHV1 and herpesvirus particles in neurons, glial cells, tongue mucosal epithelium, and hepatocytes. PCR confirmed HuAHV1 infection. These findings illustrate how disruption of the One Health equilibrium in anthropized environments poses risks for interspecies virus transmission with potential spillover not only from animals to humans but also from humans to free-ranging nonhuman primates or other animals.

Highly Versatile, Non-Invasive Method for Collecting Buccal DNA from Free-Ranging Non-Human Primates

Non-invasive techniques for collection of DNA samples of suitable quality and quantity are important for improving the efficiency of genetic wildlife research. The development of a non-invasive method for collection of DNA samples from wild stump-tailed macaques (Macaca arctoides) is described herein. Sterilized polyester rope was cut into 10 cm pieces, which were then soaked in a 20% sugar solution to bait individuals. Rope swabs were immediately collected and transferred to a lysis buffer solution after subjects had picked up, chewed and discarded them. DNA was later extracted from the buffer. Quantitative real-time PCR and both allelic dropout and genotype failure rates were used to compare the quantity and quality of the buccal DNA samples to those of intestinal slough cell DNA samples collected from freshly dropped feces. The buccal samples yielded significantly more DNA (27.1 ± 33.8 ng/μL) than did the fecal samples (11.4 ± 15.4 ng/μL) and exhibited lower allelic dropout and genotyping failure rates for the 10 autosomal microsatellites investigated. Buccal cell collection was also simple, inexpensive, reliable and less time-consuming compared to fecal sampling. Thus, this method should facilitate genome-wide studies of non-human primates and other wildlife species.

Soil-transmitted helminth infections in free-ranging non-human primates from Cameroon and Gabon

BackgroundZoonotic diseases are a serious threat to both public health and animal conservation. Most non-human primates (NHP) are facing the threat of forest loss and fragmentation and are increasingly living in closer spatial proximity to humans. Humans are infected with soil-transmitted helminths (STH) at a high prevalence, and bidirectional infection with NHP has been observed. The aim of this study was to determine the prevalence, genetic diversity, distribution and presence of co-infections of STH in free-ranging gorillas, chimpanzees and other NHP species, and to determine the potential role of these NHP as reservoir hosts contributing to the environmental sustenance of zoonotic nematode infections in forested areas of Cameroon and Gabon.MethodsA total of 315 faecal samples from six species of NHPs were analysed. We performed PCR amplification, sequencing and maximum likelihood analysis of DNA fragments of the internal transcribed spacer 2 (ITS2) nuclear ribosomal DNA to detect the presence and determine the genetic diversity of Oesophagostomum spp., Necator spp. and Trichuris spp., and of targeted DNA fragments of the internal transcribed spacer 1 (ITS1) to detect the presence of Ascaris spp.ResultsNecator spp. infections were most common in gorillas (35 of 65 individuals), but also present in chimpanzees (100 of 222 individuals) and in one of four samples from greater spot-nosed monkeys. These clustered with previously described type II and III Necator spp. Gorillas were also the most infected NHP with Oesophagostomum (51/65 individuals), followed by chimpanzees (157/222 individuals), mandrills (8/12 samples) and mangabeys (7/12 samples), with O. stephanostomum being the most prevalent species. Oesophagostomum bifurcum was detected in chimpanzees and a red-capped mangabey, and a non-classified Oesophagostomum species was detected in a mandrill and a red-capped mangabey. In addition, Ternidens deminutus was detected in samples from one chimpanzee and three greater spot-nosed monkeys. A significant relative overabundance of co-infections with Necator and Oesophagostomum was observed in chimpanzees and gorillas. Trichuris sp. was detected at low prevalence in a gorilla, a chimpanzee and a greater spot-nosed monkey. No Ascaris was observed in any of the samples analysed.ConclusionsOur results on STH prevalence and genetic diversity in NHP from Cameroon and Gabon corroborate those obtained from other wild NHP populations in other African countries. Future research should focus on better identifying, at a molecular level, the species of Necator and Oesophagostomum infecting NHP and determining how human populations may be affected by increased proximity resulting from encroachment into sylvatic STH reservoir habitats.Graphical

Detection of antibodies against Icoaraci, Ilhéus, and Saint Louis Encephalitis arboviruses during yellow fever monitoring surveillance in non-human primates (Alouatta caraya) in southern Brazil.

Free-ranging non-human primates (NHPs) can host a variety of pathogenic microorganisms, such as arboviruses, which include the yellow fever virus (YFV). This study aimed to detect the circulation of YF and other arboviruses in three wild Alouatta caraya populations in forests in southern Brazil. We collected 40 blood and serum samples from 26 monkeys captured/recaptured up to four times from 2014 to 2016, searching for evidence of arboviruses by virus isolation, PCR, and neutralization tests. Viral isolation and genome detection were negative; however, we detected neutralizing antibodies against the Saint Louis, Ilhéus, and Icoaraci viruses in three NHPs. Saint Louis Encephalitis, Ilhéus, and Icoaraci viruses circulated recently in the region. Future studies should investigate the role of NHPs, other vertebrate hosts and wild vectors in the region's arbovirus circulation and the potential risks of the arboviruses to wildlife, domestic animals, and humans.

Detection, Identification, and Antimicrobial Susceptibility of Campylobacter spp. and Salmonella spp. from Free-Ranging Nonhuman Primates in Sri Lanka

Infections with Campylobacter spp. and Salmonella spp. are the most frequently reported causes of human bacterial enteritis. Warm-blooded animals, including livestock, pets, and wildlife, can be carriers of the bacteria and may contaminate the environment and food products. The present study investigated the occurrence of Campylobacter spp. and Salmonella spp. in fecal pat samples from free-ranging toque macaques (Macaca sinica) and tufted gray langurs (Semnopithecus priam) collected in March-May 2015 in Sri Lanka. In 58 samples from toque macaques, Campylobacter jejuni was isolated in 10 (17%), Campylobacter coli in four (7%), and Salmonella enterica subsp. enterica serovar Virchow in two (3%). None of the bacteria were isolated in the 40 samples from tufted gray langurs. Pulse-field gel electrophoresis and multilocus sequence typing identified six profiles and four clonal complexes of C. jejuni. The isolated Campylobacter spp. showed varying susceptibility to antimicrobial substances. All Campylobacter spp. isolates were susceptible to chloramphenicol, erythromycin, florfenicol, gentamicin, and streptomycin. Four of the C. jejuni were resistant to at least one of the following: ampicillin, ciprofloxacin, nalidixic acid, and tetracycline, and one of the isolates was multidrug resistant. All four C. coli were resistant to ampicillin, whereas the two Salmonella Virchow strains were susceptible to all antibiotics tested. The presence of Campylobacter spp. and Salmonella spp. in toque macaques may have an impact on the conservation of endangered primates and public health in Sri Lanka.

Detection of the mosquito-borne flaviviruses, West Nile, Dengue, Saint Louis Encephalitis, Ilheus, Bussuquara, and Yellow Fever in free-ranging black howlers (Alouatta caraya) of Northeastern Argentina.

Several medically important mosquito-borne flaviviruses have been detected in Argentina in recent years: Dengue (DENV), St. Louis encephalitis (SLEV), West Nile (WNV) and Yellow Fever (YFV) viruses. Evidence of Bussuquara virus (BSQV) and Ilheus virus (ILHV) activity were found, but they have not been associated with human disease. Non-human primates can act as important hosts in the natural cycle of flaviviruses and serological studies can lead to improved understanding of virus circulation dynamics and host susceptibility. From July–August 2010, we conducted serological and molecular surveys in free–ranging black howlers (Alouatta caraya) captured in northeastern Argentina. We used 90% plaque-reduction neutralization tests (PRNT90) to analyze 108 serum samples for antibodies to WNV, SLEV, YFV, DENV (serotypes 1and 3), ILHV, and BSQV. Virus genome detection was performed using generic reverse transcription (RT)-nested PCR to identify flaviviruses in 51 antibody-negative animals. Seventy animals had antibodies for one or more flaviviruses for a total antibody prevalence of 64.8% (70/108). Monotypic (13/70, 19%) and heterotypic (27/70, 39%) patterns were differentiated. Specific neutralizing antibodies against WNV, SLEV, DENV-1, DENV-3, ILHV, and BSQV were found. Unexpectedly, the highest flavivirus antibody prevalence detected was to WNV with 9 (8.33%) monotypic responses. All samples tested by (RT)-nested PCR were negative for viral genome. This is the first detection of WNV-specific antibodies in black howlers from Argentina and the first report in free-ranging non-human primates from Latin-American countries. Given that no animals had specific neutralizing antibodies to YFV, our results suggest that the study population remains susceptible to YFV. Monitoring of these agents should be strengthened to detect the establishment of sylvatic cycles of flaviviruses in America and evaluate risks to wildlife and human health.

Optimization of a Novel Non-invasive Oral Sampling Technique for Zoonotic Pathogen Surveillance in Nonhuman Primates.

Free-ranging nonhuman primates are frequent sources of zoonotic pathogens due to their physiologic similarity and in many tropical regions, close contact with humans. Many high-risk disease transmission interfaces have not been monitored for zoonotic pathogens due to difficulties inherent to invasive sampling of free-ranging wildlife. Non-invasive surveillance of nonhuman primates for pathogens with high potential for spillover into humans is therefore critical for understanding disease ecology of existing zoonotic pathogen burdens and identifying communities where zoonotic diseases are likely to emerge in the future. We developed a non-invasive oral sampling technique using ropes distributed to nonhuman primates to target viruses shed in the oral cavity, which through bite wounds and discarded food, could be transmitted to people. Optimization was performed by testing paired rope and oral swabs from laboratory colony rhesus macaques for rhesus cytomegalovirus (RhCMV) and simian foamy virus (SFV) and implementing the technique with free-ranging terrestrial and arboreal nonhuman primate species in Uganda and Nepal. Both ubiquitous DNA and RNA viruses, RhCMV and SFV, were detected in oral samples collected from ropes distributed to laboratory colony macaques and SFV was detected in free-ranging macaques and olive baboons. Our study describes a technique that can be used for disease surveillance in free-ranging nonhuman primates and, potentially, other wildlife species when invasive sampling techniques may not be feasible.

Detection and characterization of zoonotic pathogens of free-ranging non-human primates from Zambia.

BackgroundWildlife may harbor infectious pathogens that are of zoonotic concern acting as a reservoir of diseases transmissible to humans and domestic animals. This is due to human-wildlife conflicts that have become more frequent and severe over recent decades, competition for the available natural habitats and resources leading to increased human encroachment on previously wild and uninhabited areas.MethodsA total of 88 spleen DNA samples from baboons and vervet monkeys from Zambia were tested for zoonotic pathogens using genus or species-specific PCR. The amplified products were then subjected to sequencing analysis.ResultsWe detected three different pathogenic agents, including Anaplasma phagocytophilum in 12 samples (13.6%), Rickettsia spp. in 35 samples (39.8%) and Babesia spp. in 2 samples (2.3%).ConclusionThe continuously increasing contacts between humans and primate populations raise concerns about transmission of pathogens between these groups. Therefore, increased medical and public awareness and public health surveillance support will be required to detect and control infections caused by these agents at the interface between humans and wildlife.

Detection and characterization of zoonotic pathogens of free-ranging non-human primates from Zambia

Wildlife may harbor infectious pathogens that are of zoonotic concern acting as a reservoir of diseases transmissible to humans and domestic animals. This is due to human-wildlife conflicts that have become more frequent and severe over recent decades, competition for the available natural habitats and resources leading to increased human encroachment on previously wild and uninhabited areas. A total of 88 spleen DNA samples from baboons and vervet monkeys from Zambia were tested for zoonotic pathogens using genus or species-specific PCR. The amplified products were then subjected to sequencing analysis. We detected three different pathogenic agents, including Anaplasma phagocytophilum in 12 samples (13.6%), Rickettsia spp. in 35 samples (39.8%) and Babesia spp. in 2 samples (2.3%). The continuously increasing contacts between humans and primate populations raise concerns about transmission of pathogens between these groups. Therefore, increased medical and public awareness and public health surveillance support will be required to detect and control infections caused by these agents at the interface between humans and wildlife.

Daily activity and light exposure levels for five species of lemurs at the duke lemur center

Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24-hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light-dark exposure and activity-rest patterns in free-ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter-D pendant that contained light and accelerometer sensors. Our results reveal common as well as species-specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre-sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid-day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species-specific photic niches and behaviors. The eventual application of the Daysimeter-D in the wild may help to better understand the adaptive evolution of ancestral primates.

Prevalence of Babesia microti in Free-Ranging Baboons and African Green Monkeys

Babesia microti-like parasites have been reported to infect captive non-human primates (NHPs). However, studies on the prevalence of Babesia spp. in free-ranging NHPs are lacking. This investigation aimed at determining the prevalence of B. microti in wild-caught Kenyan NHPs. In total, 125 animals were studied, including 65 olive baboons (Papio cynocephalus anubis) and 60 African green monkeys ([AGMs] Chlorocebus aethiops). Nested polymerase chain reaction targeting Babesia β-tubulin genes was used to diagnose infection prevalence. Results indicated a prevalence of 22% (27/125) B. microti infection in free-ranging NHPs in Kenya. There was no statistically significant difference in B. microti infection prevalence between baboons and AGMs or male and female animals. This is the first report of the presence and prevalence of B. microti in free-ranging Kenyan NHPs.

Chromobacterium violaceum Infection in a Free-ranging Howler Monkey in Costa Rica

Chromobacterium violaceum is a gram-negative saprobe bacterium that is a rare opportunistic pathogen in mammals. There are numerous reports in humans including fatalities, but no record exists in free-ranging nonhuman primates. Here we report an infection by C. violaceum in a wild adult male howler monkey (Alouatta palliata) captured at Ballena Marine National Park, in southwestern Costa Rica. The individual had severe skin lesions over its extremities; gross findings included multiple skin ulcers, white foci in liver, and lymphoid hyperplasia. Histologic results included deep dermatitis with presence of necrotic epithelial cells where clusters of coccoid-shaped bacteria were detected. In the liver, numerous neutrophils forming microabscesses, telangiectasia, and focal necrotic areas were observed. Necrotic liver tissue sampled for bacteriologic culture resulted in the isolation of C. violaceum. We could not ascertain the source or mechanism of infection in this case, although infection through skin microabrasions is suspected. To the best of our knowledge, this is the first report for this pathogen in a wild, nonhuman primate. This report also draws attention to this infectious agent as a potential emerging wildlife disease and consideration should be paid by regional veterinary and epidemiologic vigilance services.

Effects of age on cerebrospinal fluid oxytocin levels in free-ranging adult female and infant rhesus macaques.

There is growing interest in examining oxytocin and social functioning in human and non-human primates. Studies of human oxytocin biology are typically restricted to peripheral assessments because opportunities to collect cerebrospinal fluid (CSF) are rare. Several studies have examined CSF oxytocin levels in captive adult primates, but none to our knowledge have been conducted under free-ranging conditions and inclusive of infants. The main goal of this study was to establish feasibility of quantifying CSF oxytocin levels in free-ranging adult female and infant rhesus monkeys living on Cayo Santiago, PR. CSF oxytocin levels were examined in relation to individuals' demographic and reproductive characteristics as well as plasma cortisol levels. CSF oxytocin concentrations ranged from 36.02 to 134.41 pg/ml in adult females (ages 7-26 years; N = 31) and 35.94 to 77.3 pg/ml in infants (ages 38-134 days; N = 17). CSF oxytocin levels were positively correlated with adult female age and negatively correlated with infant age. The former correlation was driven by reproductive status. CSF oxytocin levels were unrelated to dominance rank or plasma cortisol levels. In contrast to a previous study of plasma oxytocin concentrations in this population, CSF oxytocin levels did not differ significantly between lactating and non-lactating females. These findings: 1) provide feasibility data for examining CSF oxytocin levels in free-ranging non-human primates and 2) indicate that CSF oxytocin levels may be a biomarker of age-related central nervous system changes across lifespan development. Research is now required to examine CSF oxytocin levels in the context of social functioning in free-ranging rhesus monkeys.

Synanthropic primates in Asia: potential sentinels for environmental toxins.

Macaques are similar to humans both physiologically and behaviorally. In South and Southeast Asia they are also synanthropic, ecologically associated with humans. Synanthropy with humans raises the possibility that macaques come into contact with anthropogenic toxicants, such as lead and mercury, and might be appropriate sentinels for human exposures to certain toxic materials. We measured lead (Pb) and mercury (Hg) levels and characterized the stable isotopic compositions of delta(15)N and delta(13)C in hair from three groups of free-ranging macaques at the Swoyambhu temple in Kathmandhu, Nepal, an urban population that has abundant contact with humans. Hair lead levels were significantly higher among young macaques and differed among the three groups of macaques that were sampled. Hair Hg levels were low. No statistical association was found between stable isotopic compositions (delta(15)N and delta(13)C) and Pb and Hg levels. Our data did not find evidence that lead levels were associated with diet. We conclude that, in this population of macaques, behavioral and/or physiologic factors may play a significant role in determining exposure to lead. Chemical analysis of hair is a promising, noninvasive technique for determining exposure to toxic elements in free-ranging nonhuman primates.

Sensitive Assays for Simian Foamy Viruses Reveal a High Prevalence of Infection in Commensal, Free-Ranging Asian Monkeys

Foamy viruses (FV) are retroviruses that naturally infect many hosts, including most nonhuman primates (NHPs). Zoonotic infection by primate FV has been documented in people in Asia who reported contact with free-ranging macaques. FV transmission in Asia is a concern, given abundant human-NHP contact, particularly at monkey temples and in urban settings. We have developed three assays capable of detecting the presence of FV in Asian NHP species that are commensal with humans: enzyme-linked immunosorbent assay (ELISA), Western blot assays using recombinant viral Gag protein, and an indicator cell line that can detect macaque FV. The recombinant ELISA correlates very well with the presence of FV sequences detected by PCR. We have used these assays to demonstrate both that FV is highly prevalent among free-ranging NHPs and that seroconversion occurs at a young age in these animals. These assays should also prove useful for large-scale analysis of the prevalence of FV infections in human populations in Asia that are commensal with free-ranging NHPs.

Disease risk analysis: a tool for primate conservation planning and decision making

Concern about emerging and re-emerging diseases plays an increasing role in conservation and management of both captive and free-ranging nonhuman primates (NHPs). Managers and policy makers must formulate conservation plans in an arena plagued by uncertainty, complexity, emotion, and politics. The risk analysis paradigm provides a framework that brings together scientists and policy experts to make better decisions for both people and animals. Risk analysis is a multidisciplinary, science-based process that provides an organized and logical approach for incorporating scientific information into policy development in the real world. By blending four specific goal-oriented stages-hazard identification, risk assessment, risk management, and risk communication-one can logically assess the probability that an adverse event, such as the introduction of an emerging disease into a naïve population, will occur. The following is a review of this process as it pertains to NHP conservation and risks associated with infectious diseases.

Kinship and behavior in primates

Contributors 1: Bernard Chapais and Carol M. Berman: Introduction: The Kinship Black Box Part I. Who Are Kin? Methodological Advances in Determining Kin Relationships 2: Philip A. Morin and Tony L. Goldberg: Determination of Genealogical Relationships from Genetic Data: A review of Methods and Applications 3: David S. Woodruff: Noninvasive Genotyping and Field Studies of Free-Ranging Nonhuman Primates Part II. Kin Compositions: Ecological Determinants, Population Genetics, and Demography 4: Lynne A. Isbell: Is There No Place Like Home? Ecological Bases of Female Dispersal and Philopatry and Their Consequences for the Formation of Kin Groups 5: Guy A. Hoelzer, Juan Carlos Morales, and Don J. Melnick: Dispersal and the Population Genetics of Primate Species 6: David A. Hill: The Effects of Demographic Variation on Kinship Structure and Behavior in Cercopithecines Part III. Diversity of Effects of Kinship on Behavior 7: Ellen Kapsalis: Matrilineal Kinship and Primate Behavior 8: Karen B. Strier: Patrilineal Kinship and Primate Behavior 9: Leanne T. Nash: Kinship and Behavior Among Nongregarious Nocturnal Prosimians: What Do We Really Know? 10: James Dietz: Kinship Structure and Reproductive Skew in Cooperatively Breeding Primates 11: Fernando Colmenares: Kinship Structure and Its Impact on Behavior in Multilevel Societies 12: Andreas Paul and Jutta Kuester: The Impact of Kinship on Mating and Reproduction Part IV. Kin Bias: Proximate and Functional Processes 13: Drew Rendall: Recognizing Kin: Mechanisms, Media, Minds, Modules, and Muddles 14: Carol M. Berman: Developmental Aspects of Kin Bias in Behavior 15: Dorthy L. Cheyney and Robert M. Seyfarth: The Recognition of Other Individuals' Kinship Relationships 16: Bernard Chapais and Patrick Belisle: Constraints on Kin Selection in Primate Groups Part IV. The Evolutionary Origins of Human Kinship 17: Lars Rodseth and Richard Wrangham: Human Kinship: A Continuation of Politics by Other Means? 18 Residence Groups Among Hunter-Gatherers: A View of the Claims and Evidence for Patrilocal Bands: Helen Perich Alvarez: 19 Mating, Parenting, and the Evolution of Human Pair Bonds: Kristen Hawkes: Conclusion 20 Variation in Nepotistic Regimes and Kin Recognition: A Major Area for Future Research: Bernard Chapais and Carol M. Berman: Species Index Subject Index

CSF 5-HIAA, testosterone, and sociosexual behaviors in free-ranging male rhesus macaques in the mating season

This study examines sexual behavior, serotonin turnover in the central nervous system, and testosterone in free-ranging non-human primates. Study subjects were 33 young adult male rhesus macaques ( Macaca mulatta) living in naturalistic social groups on a 475-acre South Carolina barrier island. Blood and cerebrospinal fluid (CSF) samples were obtained during random trappings, and the subjects were located for observation by radio telemetry. Quantitative behavioral samples totaling 203 observation hours were taken during two mating seasons (September through January) in 1994 and 1995. Control observations (65 h) on 13 subjects were also taken during the non-mating seasons in 1994 and 1995. The results indicate that CSF 5-hydroxyindoleacetic acid (5-HIAA), CSF testosterone, and plasma testosterone concentrations increase significantly during the mating season. During the mating season, there were significant increases in high intensity aggression, low intensity aggression, grooming behavior, and heterosexual mounting. In the mating season, CSF 5-HIAA was significantly correlated with several sociosexual behaviors: consorts per hour, heterosexual mounts per hour, and inseminations per hour. In contrast to previous findings from the non-mating season, CSF 5-HIAA was not correlated with any measures of aggression or sociality, although during consorting, CSF 5-HIAA was positively correlated with grooming. From these findings, we conclude that the lack of correlation between intense and severe aggression and CSF 5-HIAA in the mating season may reflect the use of high intensity aggression in `normative' male-male competition over access to reproductively active females. We also conclude that CNS serotonin turnover is positively correlated with sexual competence, i.e. males with low CSF 5-HIAA concentrations are less sexually competent than males with higher concentrations. © 1997 Elsevier Science Ireland Ltd.