Caged rhesus macaques voluntarily work for ordinary food

Eight single-caged adult rhesus macaques were given the choice of freely collecting their standard food ration, i.e. 33 biscuits, from an ordinary food box or working for its retrieval from a custom-made food puzzle. During a one-hour observation session following the simultaneous distribution of biscuits in both feeders, individuals spent on average a total of 32 sec retrieving 29.0 biscuits from the food box, and 673 sec retrieving 11.3 biscuits from the food puzzle. It was inferred that the animals voluntarily worked for ordinary food, with the expression of foraging activities serving as its own reward.     

Absence of deleterious effects of inbreeding in rhesus macaques

The limited availability of rhesus macaques through importation and the need for large numbers of them for use in biomedical research in this country have led to large- scale efforts to breed them domestically in captive groups. Since gene flow into the groups is usually restricted, consanguineous inbreeding can lead to inbreeding depression, which is characterized by increases in mortality, declines in fertility, and reductions in traits associated with physiological efficiency. For this reason, it is desirable to determine the level of inbreeding at which inbreeding depression occurs in rhesus macaques. I compared fertility, mortality, and the rate of weight gain in inbred and noninbred rhesus monkeys in three captive groups. There is no evidence of inbreeding depression in rhesus macaques whose inbreeding coefficients are ≤ 0.125, a level at which inbreeding depression is known to occur in some species.     

Diet and feeding behavior of semi-free ranging mandrills in an enclosed gabonais forest

Twelve wild born mandrills (Mandrillus sphinx), six males, six females, were studied in a 1.4-ha forest enclosure in Gabon Africa. Seventy-six percent of their food was obtained from the ground (45% unidentified food objects foraged from the leaf litter, 21% from ground plants, and 10% animal matter) while 23% was taken from arboreal sources (10% from trees, 10% from vines, and 3% from shrubs). Plant parts eaten include seeds, roots, fruits, stem pith, apical branch ends, mature and immature leaves, nuts, buds, blossoms, and bark. There were significant dietary differences between sexes. There were also individual dietary differences both in preferred foods and arboreal vs terrestrial foraging locations. At nearly all times of the day at least 70% of the study group was on the ground. Sixty-four percent of their time was spent feeding, with females spending more time feeding than males. High rates of feeding were seen throughout the day, with high individual variances, which is explained by individual food preferences and a temporal partitioning of the food resources. These findings are compared to those observed in wild mandrills and other baboons.     

Seasonal patterns of food limitation in Daphnia galeata: separating food quantity and food quality effects

Food limitation for the cladoceran Daphnia galeta was measuredgrowing them with natural lake seston for one growing seasonunder standardized conditions in the laboratory. Growth rateswere related to several measures of food quantity. Particulateorganic carbon (POC) <30 µm was the best predictorof total food availability measured. It was better than chlorophyll-a(Chl-a) of the same size fraction, algal volume calculated fromcell counts or total particle volume from Coulter Counter measurements.Daphnids were also grown with Scenedesmus acutus under the sameconditions and their growth rates were compared. Sestonic carbonconcentrations were related to Scenedesmus carbon concentrations,that provided equal growth rates. The ratio of the carbon concentrationsof both food types (seston, Scenedesmus) represented the foodquality of seston. Thus, the nutritional quality of naturallake seston relative to a standard alga was determined overone growing season. Growth rates of seston fed animals revealedthat they were food limited during long periods of the year.This was also ascertained by standard clutch sizes of fieldanimals. However, the causes of food limitation varied withinthe duration of the studied period. Whereas during the clear-waterphase the food quantity was limiting (while the quality washigh: 100% Scenedesmus), shortly after on 10 June and 17 Junefood conditions were close to threshold concentrations due tolow food quality. For the remainder of the summer, a POC of0.3–0.6 mg C I^–1 with a quality of     

Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

The hypothalamic–pituitary–adrenal (HPA) axis modulates individuals' physiological responses to social stress, which is an inevitable aspect of the daily lives of group‐living animals. Previous nonhuman primate studies have reported that sex, age, rank, and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free‐ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty‐two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low‐ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low‐ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free‐ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season. Am. J. Primatol. 72:559–565, 2010. © 2009 Wiley‐Liss, Inc.     

Physiological and behavioral effects of social introduction on adult male rhesus macaques

Pair housing of laboratory macaques is widely considered to lead to positive changes in well-being, yet the process of introduction is viewed as potentially stressful and risk-prone. Behavioral and physiological data were collected on eight adult male rhesus macaques before, during, and after the process of introduction, in order to measure the initial stress of introduction as well as long-term changes in well-being. Socially experienced subjects, all implanted with biotelemetry devices, were studied in five successive phases: baseline (singly housed), 1 day each of protected contact and full contact introduction, post-introduction (1-3 weeks after introduction), and settled pairs (> or =20 weeks after introduction). One hundred and seventy-six hours of behavioral data and 672 hr of heart rate data were analyzed. Fecal cortisol was also measured for the baseline, post-introduction, and settled pair phases. All introductions were successful and subjects showed no physiological or behavioral signs of stress, such as increased heart rate, abnormal behavior, or psychological indices of distress (depressive/anxiety-related behavior). Agonism was minimal throughout the introduction process and over the subsequent months; only one wound was incurred over the course of the study. Levels of abnormal behaviors, psychological indices of distress, locomotion, inactivity, and affiliation showed improvements within several weeks after introduction; these changes were still present 5-9 months later for the latter two categories. Heart rates during introduction fell significantly in the settled pair phase, and also varied predictably with time of day. Fecal cortisol levels were lower in settled pairs than in single housing. The fact that reductions in abnormal behavior did not persist over the long term may have been confounded by increasing duration of time spent caged. The results of this study may be of practical use for designing and monitoring social introductions and suggest that managers should not dismiss the feasibility of successful pairing of adult male rhesus macaques.     

Affiliative and submissive communication in rhesus macaques

This study analyzed the occurrence of selected facial expressions, gestures, and postures, in relation to sex and rank of sender and receiver, context, and responses elicited in a large multi-male multi-female group of rhesus macaques (Macaca mulatta) living in captivity. The group was observed for 100 hr during the mating and the birth season. Data were collected with the behavior sampling method. The bared-teeth display and the hindquarter presentation were the most prominent signals in the rhesus submissive and affiliative repertoire. Both signals were primarily displayed in response to aggression and approaches; bared-teeth in response to approaches from the front, presentation in response to approaches from the rear. Lip-smack had a submissive component like baredteeth and presentation but was more likely to be displayed by approaching individuals and followed by affiliation than these behaviors. The distribution of hip-touch and mount was different from that of bared-teeth, presentation, and lip-smack, these behaviors mostly occurring between males, irrespective of their dominance rank. Other infrequent signals and behavioral sequences were limited to specific male-female and mother-infant interactions.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Voles on small islands: effects of food limitation and alien predation

Ecosystems of three trophic levels may be bottom-up (by food-plant availability) and/or top-down (by predators) limited. Top-down control might be of greater consequence when the predation impact comes from an alien predator. We conducted a replicated two-factor experiment with field voles (Microtus agrestis) during 2004-2005 on small islands of the outer archipelago of the Baltic Sea, south-west Finland, manipulating both predation impact by introduced American mink (Mustela vison) and winter food supply. In autumn 2004, we live-trapped voles on five islands from which mink had been consistently removed, and on four islands where mink were present, and provided half of these islands with 1.8 kg oats per vole. Body mass of female voles increased as a response to supplementary food, whereas both food supplementation and mink removal increased the body mass of male voles in subsequent spring. During winter, there was a positive effect of supplementary food, but in the subsequent summer, possible positive long-term impacts of food supplementation on field voles were not detected. Mink removal appeared not to affect density estimates of field voles during the winter and summer immediately after food addition. Trapping data from 2004 to 2005 and 2007 suggested, however, that in two out of three summers densities of voles were significantly higher in the absence than in the presence of mink. We conclude that vole populations on small islands in the archipelago of the Baltic Sea are mainly bottom-up limited during winter (outside the growing season of food plants), when food availability is low, and limited by mink predation during summer which slows population growth during the reproductive season of voles.     

Larval food limitation in butterflies: effects on adult resource allocation and fitness

Allocation of larval food resources affects adult morphology and fitness in holometabolous insects. Here we explore the effects on adult morphology and female fitness of larval semi-starvation in the butterfly Speyeria mormonia. Using a split-brood design, food intake was reduced by approximately half during the last half of the last larval instar. Body mass and forewing length of resulting adults were smaller than those of control animals. Feeding treatment significantly altered the allometric relationship between mass and wing length for females but not males, such that body mass increased more steeply with wing length in stressed insects as compared to control insects. This may result in changes in female flight performance and cost. With regard to adult life history traits, male feeding treatment or mating number had no effect on female fecundity or survival, in agreement with expectations for this species. Potential fecundity decreased with decreasing body mass and relative fat content, but there was no independent effect of larval feeding treatment. Realized fecundity decreased with decreasing adult survival, and was not affected by body mass or larval feeding treatment. Adult survival was lower in insects subjected to larval semi-starvation, with no effect of body mass. In contrast, previous laboratory studies on adult nectar restriction showed that adult survival was not affected by such stress, whereas fecundity was reduced in direct 11 proportion to the reduction of adult food. We thus see a direct impact of larval dietary restriction on survival, whereas fecundity is affected by adult dietary restriction, a pattern reminiscent of a survival/reproduction trade-off, but across a developmental boundary. The data, in combination with previous work, thus provide a picture of the intra-specific response of a suite of traits to ecological stress.     

Androgen binding in peripheral tissues of fetal rhesus macaques: effects of androgen metabolism in liver

In rhesus monkeys sexual differentiation of the brain and reproductive tract (RT) is androgen-dependent. Presumably these effects are mediated through the androgen receptor (AR). The AR has not been characterized in fetal tissues such as liver, kidney, heart, spinal cord and RT in this species. We characterized AR binding using [3H]R1881 as the ligand in cytosols from tissues obtained on days 100-138 of gestation. Scatchard analyses revealed a single, saturable, high affinity AR in liver, kidney, heart, spinal cord and RT. The apparent dissociation constant (Kd) ranged from 0.52 to 0.85 nM with no significant tissue differences. The number of AR (Bmax; fmol/mg protein) differed significantly (P less than 0.01) between tissues (liver greater than RT much greater than kidney greater than or equal to heart greater than or equal to spinal cord). Radioinert testosterone (T) and 5 alpha-dihydrotestosterone (DHT) but not androstenedione, progesterone, estradiol-17 beta, estrone or cortisol in a 50-fold molar excess inhibited [3H]R1881 binding to the AR in spinal cord, heart, kidney and RT. However, in liver only DHT competed significantly (P less than 0.01) for binding. This difference in binding of DHT vs T in the liver was further investigated by incubating liver and kidney cytosols with [3H]DHT and [3H]T at 4 degrees C. We identified the metabolic products by mobility on Sephadex LH-20 columns and reverse isotope dilution. Liver cytosols metabolized [3H]DHT to 5 alpha-androstane- 3 alpha,17 beta-diol (5 alpha-diol) and [3H]T to 5 beta-androstane-3 alpha, 17 beta-diol (5 beta-diol) at 4 degrees C. In contrast, kidney cytosols metabolized [3H]DHT while [3H]T remained unchanged. Further studies indicated that a 50-fold molar excess of 5 alpha-diol inhibited the binding of [3H]R1881 in liver cytosols by about 50% whereas the same molar concentration of 5 beta-diol had no effect. These data demonstrate the presence of AR in peripheral tissues of fetal rhesus monkeys and suggest that androgens through their receptors may affect development of these tissues. Liver cytosols are capable of metabolizing T and DHT at 4 degrees C at conditions similar to those used for measuring cytosolic AR. However, T and DHT are metabolized differently, generating different isomers which have different affinities for hepatic AR.     

Social behavior in aged rhesus macaques

This study investigated the relationship between chronological age and social behavior in 42 adult male and female rhesus macaques (Macaca mulatta) in three specific areas: social interactions, social roles, and social networks. While both old males and old females share behavioral differences associated with senescence, this study reports that old females and old males are distinct in their social behaviors, both from each other and from other adults. Many of these differences appear progressive across age classes, e.g., declining across age classes in females and increasing across age classes in males. Old females are less social and have smaller social networks than other females, while the opposite was found to be true of old males. An explanation for the sex-based differences in aged social behavior and social networks reported in this study may originate in rhesus matrifocal social structure.     

Assisted reproductive technologies in rhesus macaques

The assisted reproductive technologies (ARTs) have been used in the production of rhesus monkey offspring at the Oregon National Primate Research Center (ONPRC) and that experience is summarized here. Additionally these technologies serve as a source of oocytes/embryos for monozygotic twinning, embryonic stem (ES) cell derivation and cloning. High fertilization efficiencies were realized with conventional insemination or following the use of intracytoplasmic sperm injection (ICSI) and approximately 50% of the resulting embryos grew in vitro to blastocysts. Both fresh and frozen sperm were employed in fertilization by ICSI and the resulting embryos could be low temperature stored for subsequent thawing and transfer when a synchronized recipient female was available or after shipment to another facility. Following the transfer of up to 3 embryos, an overall pregnancy rate of 30% was achieved with increasing rates dependent upon the number of embryos transferred. Singleton pregnancy outcomes following the transfer of ART produced embryos were similar to those observed in a control group of animals in the timed mated breeding colony at ONPRC. ICSI produced embryos were used in efforts to create monozygotic twins by blastomere separation or blastocyst splitting. While pregnancies were achieved following the transfer of demi-embryos, only one was a twin and it was lost to spontaneous abortion. ICSI produced embryos have also served as the source of blastocysts for the derivation of embryonic stem cells. These pluripotent cells hold potential for cell based therapies and we consider the monkey an important translational model in which to evaluate safety, efficacy and feasibility of regenerative medicine approaches based on the transplantation of stem cell-derived progeny. Finally, efforts to produce genetically-identical monkeys by nuclear transfer have been briefly summarized.     

Dominance style of Japanese macaques compared with rhesus and stumptail macaques

In the present study, we seek to relate dominance style with group cohesion in a captive group of Japanese macaques (Macaca fuscata). Social data were gathered on approach rate, result, and direction, aggression rate and intensity, grooming rate and direction, and conciliatory tendency. Data were collected using focal animal sampling and instantaneous scan sampling. Reconciliation data were collected using ad libitum observations of aggression with ten-minute post-conflict and matched-control focal observations. Data were compared to prior studies on rhesus (M. mulatta) and stumptail macaques (M. arctoides) living in similar environments. Each species demonstrated the presence of a formalized dominance hierarchy based on the teeth-baring display. The Japanese macaque group showed a lower rate of approach with a higher proportion of negative outcomes than either of the other species. Rates of aggression and reconciliation were also lower in the study troop, suggesting a strict hierarchy while maintaining an optimal nearest-neighbor distance. Overall, this group of Japanese macaques was less sociable than other groups of the same species, perhaps due to a history of individual removals. © 1995 Wiley-Liss, Inc.