Captive Monkeys Research Articles

Variation in Scrotal Color Among Widely Distributed Vervet Monkey Populations (Chlorocebus Aethiops Pygerythrus and Chlorocebus Aethiops Sabaeus)

Vervet monkeys (Chlorocebus aethiops) exhibit bright blue scrotal skin which may function to mediate social interactions by acting as a socio-sexual signal. Previous research on scrotal coloration among vervet monkeys was limited to experimental work on captive Ch. a. sabaeus, the least colorful vervet subspecies, and two field studies of the more colorful Ch. a. pygerythrus. In a study of free-ranging and captive vervet monkeys in South Africa (Ch. pygerythrus), West Africa (Ch. a. sabaeus) and the Caribbean (Ch. a. sabaeus), we examined scrotal color variation across geographically distant subspecies. We provide an exploration of how digital photographs may be used to quantify and analyze blue and green skin coloration by examining the blue-yellow opponency channel and luminance channel as color measures. We found that that at all ages the scrotal color of Ch. a. pygerythrus males was always bluer and darker than that of Ch. a. sabaeus males. Among Ch. a. pygerythrus scrotal color becomes bluer and lightens with increasing age, while the color of Ch. a. sabaeus males also lightens, but becomes less blue with increasing age. We suggest that color variation is related to maturation and may function as an age-related signal among Ch. a. pygerythrus and Ch. a. sabaeus. We also found color was related to three morphological features among adults. For Ch. a. pygerythrus, higher body weight is associated with more blue color and longer canine length is associated with lighter color. Lighter color was associated with longer body lengths among Ch. a. sabaeus. Future studies focused on color variation within age classes are needed to examine the potential signal content of color in this species.

Functional class formation in the context of a foraging task in capuchin monkeys

Functional class formation via repeated reversals of simple discriminations was investigated in a foraging task in captive capuchin monkeys (Cebus cf. apella). Two capuchin monkeys were given simultaneous simple discrimination training and reversals with two (Phase 1), four (Phase 2), and six (Phase 3) visual stimuli (wooden boxes) in the context of searching for food in an apparatus. One different kind of food for each potential stimulus class was used as a reinforcer. After repeated functional reversals of two stimulus sets, multiple tests for functional class formation were performed (Phase 4). Evidence of class formation was found in all of the tests. Next, the same monkeys were given simultaneous simple discrimination training with variations of the stimulus locations between sessions (Phase 5). The class-specific reinforcement procedure was suspended. Tests for functional class formation were again performed. Evidence of class formation was found in all tests. The data suggest that some of the procedural difficulties in documenting class formation in nonhumans can be overcome with procedures that take advantage of the natural skills of the subjects.

Personality as a Predictor of General Health in Captive Golden Snub‐Nosed Monkeys (Rhinopithecus roxellana)

Increasing studies in human and animals have shown that personality is related to biological profile and affects health outcomes. Understanding the link between personality and health will contribute to preventing illness and promoting well-being in non-human primates. The present study examined whether personality predicted health outcomes in captive golden snub-nosed monkeys (Rhinopithecus roxellana). Personality was measured by rating on a list of traits and four factors (Aggressiveness, Sociability, Mellowness, and Excitability) were extracted. Morbidity was measured by occurrence, duration, and number of illnesses, as well as (mean and maximum) digestive dysfunction symptoms scores. Morbidity measurements were coded from illness history which was recorded during the 27 months since the personality assessment. The results showed that lower Aggressiveness predicted greater number of illness, longer illness duration, and more serious digestive dysfunction. In addition, Mellowness, Excitability, and age by Sociability interaction influenced digestive function significantly. Low mellow individuals, high excitable individuals, high sociable younger individuals and low sociable older individuals had poorer digestive function. The present study demonstrated that personality was associated with morbidity in captive R. roxellanae and stress might contribute to this association. Personality assessment provided useful information on individual vulnerability. Carefully looking for early signs of illness among vulnerable individuals is expected to reduce health risks, which would promote welfare in captive non-human primates.

Quantitative genetics of costly neonatal sexual size dimorphism in squirrel monkeys (Saimiri boliviensis).

Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex-specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.

Systems Biology of the Vervet Monkey

Nonhuman primates (NHP) provide crucial biomedical model systems intermediate between rodents and humans. The vervet monkey (also called the African green monkey) is a widely used NHP model that has unique value for genetic and genomic investigations of traits relevant to human diseases. This article describes the phylogeny and population history of the vervet monkey and summarizes the use of both captive and wild vervet monkeys in biomedical research. It also discusses the effort of an international collaboration to develop the vervet monkey as the most comprehensively phenotypically and genomically characterized NHP, a process that will enable the scientific community to employ this model for systems biology investigations.

Identification of sperm head subpopulations with defined pleiomorphic characteristics in ejaculates of captive Goeldi's monkeys (Callimico goeldii)

The aim of this study was to evaluate the incidence of pleiomorphisms and its influence on the distribution of sperm morphometric subpopulations in ejaculates from the vulnerable Goeldi's monkey (Callimico goeldii) by using a combination of computerized analysis system and Principal Component Analysis (PCA) methods. Each sperm head was measured for four primary spermatozoal head dimensional parameters (area [A (μm2)], perimeter [P (μm)], length [L (μm)] and width [W (μm)]) and three head shape derived parameters (ellipticity [(L/W)], elongation [(L−W)/(L+W)] and rugosity [(4πA/P2)]). Six separate subpopulations (SPs) were identified: SP1, constituted by very large, narrow and very elliptical spermatozoa (A=16.85±1.56μm2, W=2.75±0.42μm and ellipticity=2.16±0.24); SP2, characterized by average sized, short, wide and round spermatozoa (A=15.00±1.92μm2, L=5.06±0.49μm, W=3.51±0.31μm and ellipticity=1.44±0.15); SP3, represented by small, wide and slightly round spermatozoa (A=14.95±1.75μm2, W=3.47±0.29μm and ellipticity=1.48±0.14); SP4 included very small, short and very round spermatozoa (A=14.15±2.38μm2, L=4.90±0.57μm and elongation=0.18±0.05); SP5 consisted of average sized and slightly elliptical spermatozoa (A=15.14±1.72μm2 and ellipticity=1.49±0.14); and SP6 included large and round spermatozoa (A=16.30±1.62μm2 and elongation=0.19±0.04). There were differences in the sperm subpopulation distribution (P<0.001) among the five donors analyzed. In conclusion, the results of the current study confirmed that the use of computer sperm analysis methods combined with PCA cluster analyses are useful methods to identify, classify, and characterize different sperm head morphometric subpopulations in neotropical primates. Broadening our knowledge of C. goeldii sperm morphometric abnormalities as well as developing reliable techniques for sperm evaluation may be essential for ex situ conservation of this threatened species.

ELECTROCARDIOGRAPHIC PARAMETERS OF CAPTIVE TUFTED CAPUCHINS (CEBUS APELLA) UNDER CHEMICAL IMMOBILIZATION

This study presents the electrocardiogram findings from 97 captive tufted capuchin monkeys (Cebus apella) at the São Paulo Zoo (São Paulo, Brazil) while under ketamine anesthesia. The results did not differ greatly from data of domestic carnivores or other studied primate species. The most common rhythm recorded was normal sinus rhythm, followed by normal sinus rhythm with wandering pacemaker. Electrical axis varied from 0 degrees to -150 degrees but was most commonly between +60 degrees and +90 degrees. QRS complexes were predominantly positive in leads DI, DII, DIII, and AVF. These findings allow for the recognition of abnormal rhythms in these primate species and can contribute to future investigations into the cardiovascular diseases routinely diagnosed in primates and humans.

MOLECULAR DIAGNOSIS OFLEISHMANIA AMAZONENSISIN A CAPTIVE SPIDER MONKEY IN BAURU, SÃO PAULO, BRAZIL

The municipality of Bauru, São Paulo, Brazil, is an area endemic for leishmaniasis. At the zoo, a spider monkey (Ateles paniscus) showed nonpathognomonic symptoms, such as weight loss and pale mucous membranes. Blood was collected from the jugular vein and investigated for the presence of Leishmania spp. DNA by polymerase chain reaction and restriction fragment length polymorphism. Parasite DNA was detected, and the pattern observed was identical to Leishmania amazonensis. This study presents molecular evidence of L. amazonensis infection in a captive spider monkey.

Digestive Efficiency Mediated by Serum Calcium Predicts Bone Mineral Density in the Common Marmoset (Callithrix jacchus)

Two health problems have plagued captive common marmoset (Callithrix jacchus) colonies for nearly as long as those colonies have existed: marmoset wasting syndrome and metabolic bone disease. While marmoset wasting syndrome is explicitly linked to nutrient malabsorption, we propose metabolic bone disease is also linked to nutrient malabsorption, although indirectly. If animals experience negative nutrient balance chronically, critical nutrients may be taken from mineral stores such as the skeleton, thus leaving those stores depleted. We indirectly tested this prediction through an initial investigation of digestive efficiency, as measured by apparent energy digestibility, and serum parameters known to play a part in metabolic bone mineral density of captive common marmoset monkeys. In our initial study on 12 clinically healthy animals, we found a wide range of digestive efficiencies, and subjects with lower digestive efficiency had lower serum vitamin D despite having higher food intakes. A second experiment on 23 subjects including several with suspected bone disease was undertaken to measure digestive and serum parameters, with the addition of a measure of bone mineral density by dual-energy X-ray absorptiometry (DEXA). Bone mineral density was positively associated with apparent digestibility of energy, vitamin D, and serum calcium. Further, digestive efficiency was found to predict bone mineral density when mediated by serum calcium. These data indicate that a poor ability to digest and absorb nutrients leads to calcium and vitamin D insufficiency. Vitamin D absorption may be particularly critical for indoor-housed animals, as opposed to animals in a more natural setting, because vitamin D that would otherwise be synthesized via exposure to sunlight must be absorbed from their diet. If malabsorption persists, metabolic bone disease is a possible consequence in common marmosets. These findings support our hypothesis that both wasting syndrome and metabolic bone disease in captive common marmosets are consequences of inefficient nutrient absorption.

Epilepsy in Bolivian Black‐capped squirrel monkeys Saimiri boliviensis at ZSL London Zoo: management and implications for captive‐breeding programme

Squirrel monkeys (genus Saimiri) are species commonly kept in captivity in zoological collections. Fainting related to hypoglycaemia has been reported, and fits/seizures have also been observed relatively frequently in captive squirrel monkeys. However, as far as the authors are aware, there are no published reports of epilepsy in squirrel monkeys. Here we describe several cases of idiopathic epilepsy affecting related ♂ Bolivian Black‐capped squirrel monkeys Saimiri boliviensis at ZSL London Zoo, the management of the cases and the possible implications for the captive‐breeding programme.

Genetic variation of Gongylonema pulchrum from wild animals and cattle in Japan based on ribosomal RNA and mitochondrial cytochrome c oxidase subunit I genes

The gullet worm (Gongylonema pulchrum) has been recorded from a variety of mammals worldwide, including monkeys and humans. Due to its wide host range, it has been suggested that the worm may be transmitted locally to any mammalian host by chance. To investigate this notion, the ribosomal RNA gene (rDNA), mainly regions of the internal transcribed spacers (ITS) 1 and 2, and a cytochrome c oxidase subunit I (COI) region of mitochondrial DNA of G. pulchrum were characterized using parasites from the following hosts located in Japan: cattle, sika deer, wild boars, Japanese macaques, a feral Reeves's muntjac and captive squirrel monkeys. The rDNA nucleotide sequences of G. pulchrum were generally well conserved regardless of their host origin. However, a few insertions/deletions of nucleotides along with a few base substitutions in the ITS1 and ITS2 regions were observed in G. pulchrum from sika deer, wild boars and Japanese macaques, and those differed from G. pulchrum in cattle, the feral Reeves's muntjac and captive squirrel monkeys. The COI sequences of G. pulchrum were further divided into multiple haplotypes and two groups of haplotypes, i.e. those from a majority of sika deer, wild boars and Japanese macaques and those from cattle and zoo animals, were clearly differentiated. Our findings indicate that domestic and sylvatic transmission cycles of the gullet worm are currently present, at least in Japan.

Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans)

Western gorillas (Gorilla gorilla) have been identified as the natural reservoir of the parasites that were the immediate precursor of Plasmodium falciparum infecting humans. Recently, a P. falciparum-like sequence was reported in a sample from a captive greater spot-nosed monkey (Cercopithecus nictitans), and was taken to indicate that this species may also be a natural reservoir for P. falciparum-related parasites. To test this hypothesis we screened blood samples from 292 wild C. nictitans monkeys that had been hunted for bushmeat in Cameroon. We detected Hepatocystis spp. in 49% of the samples, as well as one sequence from a clade of Plasmodium spp. previously found in birds, lizards and bats. However, none of the 292 wild C. nictitans harbored P. falciparum-like parasites.

Digestive retention times for Allen's swamp monkey and L'Hoest's monkey: data with implications for the evolution of cercopithecine digestive strategy

Primates access energy from plant fiber via bacterial fermentation in either a modified forestomach ('foregut'), a caecocolic ('hindgut') chamber of the large intestine, or both. Longer digestive retention times allow for more complete fermentation; as such, primates that consume an herbivorous diet high in fiber are expected to have both relatively and absolutely longer retention times than those mammals that rely on more readily digestible plant foods, such as fruit. We used particulate markers to measure the digestive retention times of captive Allen's swamp monkeys [Allenopithecus nigroviridis (Pocock, 1907)] (n= 3) and L'Hoest's monkey (Cercopithecus lhoesti P. Sclater, 1899) (n= 2). Results indicate mean retention times of 23.2-29.4 h and 23.2-24.0 h for C. lhoesti and A. nigroviridus, respectively. Results from this study, in combination with previously published data on digestive retention times in other primate species, indicate that cercopithecines differ from other primate taxa by having lengthier retention times that can be predicted by body mass alone. These data are consistent with the hypothesis that relatively lengthy retention times are a primitive trait for Cercopithecinae.

Housing with Females Increases Testosterone and Cortisol Levels in Captive Groups of Black‐Handed Spider Monkeys (Ateles geoffroyi)

The black-handed spider monkey (Ateles geoffroyi) is a seasonal reproducer that requires a seclusiveness to copulate and has a fusion-fission social system. These features impose important restrictions to achieve reproduction of captive animals. We investigated if group composition in captive spider monkeys has any endocrine effects. We compared testosterone and cortisol concentrations during the mating season in all-male and multifemale-multimale groups to study if the former condition impairs reproductive potential and increases stress. Concentrations of testosterone and cortisol of males living with females were higher than those of all-male groups. In the multifemale-multimale condition, dominant males had the highest levels of testosterone, while the youngest males showed the highest concentrations of cortisol. Results show that males adjust well to isosexual grouping, this being an appropriate condition to keep animals when controlled reproduction is sought.

Establishment of a Captive All‐male Group of Proboscis Monkey (Nasalis larvatus) at the Singapore Zoo

Surplus male proboscis monkeys at the Singapore Zoo pose a considerable problem for maintenance and maximizing of exhibition potential. In 2008, a new exhibit was constructed to house and display a group of six proboscis monkey males born in Singapore Zoo. To document and monitor the all-male group establishment in the new exhibit, we conducted observations on intragroup interactions between the monkeys, spatial use of their new exhibit, and visitor effects on their behavior. We found contact aggressive interactions between the monkeys to be consistently lower than noncontact aggressive interactions and by week six of introduction to the new exhibit, contact aggression was almost nonevident. Affiliative interactions also developed between individuals in the group, with an interface of aggressive and socioreconcilatory behavior influenced by food competition and a dominance hierarchy. This was evident from significantly higher overall aggression and affiliation during feeding times compared to nonfeeding times, and this was reduced when food competition was mitigated by modifying the feeding regime. We measured the groups' spatial use of the exhibit and the relation to behavior, crowd size, and density. Our results showed that the proboscis monkeys utilized the available exhibit space, were largely unaffected by visitor crowd size and density, and were able to exhibit a variety of natural behaviors, including swimming. Our accomplishment in maintaining and displaying an all-male group of proboscis monkeys in captivity provides viable options for more comprehensive captive management and breeding programs for this endangered species.

Some stereotypic behaviors in rhesus macaques (Macaca mulatta) are correlated with both perseveration and the ability to cope with acute stressors

The most prevalent sub-group of abnormal repetitive behaviors among captive animals is that of stereotypies. Previous studies have demonstrated some resemblance between stereotypy in captive animals and in humans, including the involvement of neurological malfunctions that lead to the expression of stereotypies. This malfunction can be evaluated through the use of neuropsychological tasks that assess perseveration as implying a failure of the basal ganglia (BG) to operate properly. Other studies, in contrast, have suggested that stereotypies are the product of neurologically intact individuals reacting to the abnormal nature of their surroundings, and are possibly characterized by an adaptive feature that enables the subject to cope with such adversity. Employing neuropsychological tests and also measuring the levels of fecal corticoids in captive rhesus macaques, we tested the hypothesis that stereotypies are related both to brain pathology and to a coping mechanism with stress, resembling accounts by autistic individuals exhibiting basal ganglia malfunction, and who report a sense of relief when performing stereotypies. Self-directed and fine-motor stereotypies exhibited by the monkeys were positively correlated with perseveration, suggesting BG malfunction; while self-directed stereotypies were also negatively correlated with an increase in fecal corticoids following a stress challenge, suggesting a related coping mechanism. We therefore suggest that not all repetitive, unvarying, and apparently functionless behaviors should be regarded as one homogeneous group of stereotypic behaviors; and that, reflecting reports from autistic individuals, self-directed stereotypies in captive rhesus monkeys are related both to brain pathology, and to an adaptive mechanism that allows those that express them to better cope with acute stressors.

Allele frequency of antiretroviral host factor TRIMCyp in wild-caught cynomolgus macaques (Macaca fascicularis)

A recent study showed that the frequency of an antiretroviral factor TRIM5 gene-derived isoform, TRIMCyp, in cynomolgus macaques (Macaca fascicularis) varies widely according to the particular habitat examined. However, whether the findings actually reflect the prevalence of TRIMCyp in wild cynomolgus macaques is still uncertain because the previous data were obtained with captive monkeys in breeding and rearing facilities. Here, we characterized the TRIM5 gene in cynomolgus macaques captured in the wild, and found that the frequency of the TRIMCyp allele was comparable to those in captive monkeys. This suggests that the previous results with captive monkeys do indeed reflect the natural allele frequency and that breeding and rearing facilities may not affect the frequency of TRIM5 alleles. Interestingly, the prevalence of a minor haplotype of TRIMCyp in wild macaques from the Philippines was significantly lower than in captive ones, suggesting that it is advantageous for wild monkeys to possess the major haplotype of TRIMCyp. Overall, our results add to our understanding of the geographic and genetic prevalence of cynomolgus macaque TRIMCyp.

Changes in estrogen levels and sexual behavior in captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) following a male replacement

Changes in estrogen levels and sexual behavior in captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) following a male replacement

Captive spider monkeys (Ateles geoffroyi) arm-raise to solicit allo-grooming

Old World monkeys solicit allo-grooming from conspecifics. However, there are relatively few studies of allo-grooming among spider monkeys, and descriptions of allo-grooming solicitation among spider monkeys are anecdotal. In this study, eighty-one hours of video, shot over eight weeks, captured 271 allo-grooming bouts among small groups of captive spider monkeys. Six of eight monkeys made heretofore unreported arm-raises that solicited higher than normal rates of allo-grooming. Allo-grooming bout durations following arm-raises also tended to be longer than bouts not preceded by arm-raises. The efficacy of the arm-raise at soliciting allo-grooming suggests spider monkeys are capable of intentional communication.

Between-group hostility affects within-group interactions in tufted capuchin monkeys

Between-group competition has long been thought to be a key factor influencing within-group social dynamics. In humans, it has been suggested that between-group competition may favour the emergence of within-group cooperation. However, between-group competition can also be hypothesized to induce social tension and cause within-group social relationships to deteriorate. So far, little research has focused on these possible effects in animal societies. In this study, we used an experimental set-up to manipulate the opportunity for visual aggressive interactions between two adjacent groups of captive tufted capuchin monkeys, Cebus apella, to examine the group members’ behavioural adjustment in terms of affiliation and aggression. The ‘cooperative hypothesis’ predicted social relationships to be positively reinforced by the visual exposure to the adjacent group to buffer between-group hostility. By contrast, the ‘induced-tension hypothesis’ predicted social relationships to be negatively affected by the visual exposure to the adjacent group because of the higher level of social tension induced by between-group hostility. The experimental manipulation did not produce changes in affiliative behaviours, whereas within-group aggression was higher and the dominance hierarchy steeper when visual aggressive interactions between groups were allowed. Overall, interactions with a neighbouring group caused social relationships to deteriorate and partly confirmed the induced-tension hypothesis.