The effects of interspecies infant interaction upon social behavior ofMacaca irus andErythrocebus patas

TwoMacaca irus and twoErythrocebus patas mother-infant pairs were used as experimental subjects to test the effects of interspecies interaction upon social behavior of monkeys. Cynomolgous and patas monkeys given intraspecies interation served as control animals. An unexpected result of this study is that mother-infant behaviors were more affected by interspecies interaction than were infant-infant behaviors. The results indicate that the importance one animal has for another in the development of social behavior depends upon two factors: (a) the behavioral repertoires of interacting animals must be similar and (b) each animal must respond appropriately to the other's behavior.This research was supported in part by National Science Foundation grants No. GB4925 and GB7601 and a grant from the Louisiana State University Graduate Research Council. Animal subjects were provided by the Delta Regional Primate Research Center, United States Public Health Service grant No. FR00164 from the Division of Research Facilities and Resources.The author received personal support while conducting this research as a United States Public Health Service Trainee.     

Approach to a social stranger is associated with low central nervous system serotonergic responsivity in female cynomolgus monkeys (Macaca fascicularis)

It is widely hypothesized that individual differences in central nervous system (CNS) serotonergic activity underlie dimensional variation in "impulsive" vs. "inhibited" social behavior in both humans and nonhuman primates. To assess relative impulsivity in a social context, a behavioral challenge involving animals' exposure to a social stranger (termed the "Intruder Challenge") was recently validated in adolescent and adult male vervet monkeys (Cercopithecus aethiops sabaeus). Among these animals, monkeys that quickly approached the intruder were found to have lower cerebrospinal fluid (CSF) concentrations of the serotonin (5-HT) metabolite, 5-hydroxyindoleacetic acid, than less impulsive animals. In the present study we extended these observations to determine whether approach to a social stranger, as operationalized by the Intruder Challenge, is similarly associated with diminished CNS serotonergic function in female cynomolgus monkeys (Macaca fascicularis). Study animals were 25 adult monkeys that had been housed for 2 years in stable social groups. In each animal, the rise in plasma prolactin concentration induced by acute administration of the 5-HT agonist, fenfluramine, was used to assess "net" central serotonergic responsivity. When exposed later to an unfamiliar female of the same species in a catch-cage placed for 20 min within the subjects' home enclosure, monkeys that approached to within 1 m of the intruder (median latency to approach=3 min) were found to have significantly smaller prolactin responses to fenfluramine (diminished serotonergic responsivity) compared to "inhibited" animals that failed to approach the intruder (t=2.9, df=23, P<0.009; rpb=-0.51). Neither approach behavior nor the animals' fenfluramine-induced prolactin responses covaried significantly with nondirected expressions of arousal (or anxiety) or with aggressive behaviors exhibited during testing. We conclude that in female cynomolgus monkeys, social impulsivity (vs. inhibition) correlates inversely with individual differences in CNS serotonergic activity, as assessed by neuroendocrine challenge.     

Scavengers on the Move: Behavioural Changes in Foraging Search Patterns during the Annual Cycle

Background

Optimal foraging theory predicts that animals will tend to maximize foraging success by optimizing search strategies. However, how organisms detect sparsely distributed food resources remains an open question. When targets are sparse and unpredictably distributed, a Lévy strategy should maximize foraging success. By contrast, when resources are abundant and regularly distributed, simple Brownian random movement should be sufficient. Although very different groups of organisms exhibit Lévy motion, the shift from a Lévy to a Brownian search strategy has been suggested to depend on internal and external factors such as sex, prey density, or environmental context. However, animal response at the individual level has received little attention.

Methodology/Principal Findings

We used GPS satellite-telemetry data of Egyptian vultures Neophron percnopterus to examine movement patterns at the individual level during consecutive years, with particular interest in the variations in foraging search patterns during the different periods of the annual cycle (i.e. breeding vs. non-breeding). Our results show that vultures followed a Brownian search strategy in their wintering sojourn in Africa, whereas they exhibited a more complex foraging search pattern at breeding grounds in Europe, including Lévy motion. Interestingly, our results showed that individuals shifted between search strategies within the same period of the annual cycle in successive years.

Conclusions/Significance

Results could be primarily explained by the different environmental conditions in which foraging activities occur. However, the high degree of behavioural flexibility exhibited during the breeding period in contrast to the non-breeding period is challenging, suggesting that not only environmental conditions explain individuals'' behaviour but also individuals'' cognitive abilities (e.g., memory effects) could play an important role. Our results support the growing awareness about the role of behavioural flexibility at the individual level, adding new empirical evidence about how animals in general, and particularly scavengers, solve the problem of efficiently finding food resources.     

The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board

A new environmental enrichment device, termed a “foraging/grooming board,” was presented to 8 individually housed rhesus monkeys for the explicit purpose of reducing the level of aberrant behaviors manifested by these animals. The device, consisting of a piece of plexiglass covered with artificial fleece, had particles of food treats rubbed into it and was attached to the outside of each animal's home cage. All animals foraged from the board to the point that a significant reduction in the level of abnormal behavior was noted. Most animals also groomed the fleece covering the board, utilizing the same motor patterns that would be directed toward grooming another monkey. These boards are inexpensive to construct and easy to sanitize, and do not require placing animal facility personnel at risk to maintain them.     

Properties of arginase from liver of Macaca fascicularis: Comparison of normals with red blood cell arginase deficient monkeys

Deficiency of arginase (E.C. 3.5.3.1), the fifth enzyme of the urea cycle, was found in the red blood cells (RBCs) of Macaca fascicularis monkeys (<0.2 µmol arginine cleaved/g Hb/min; normal =49.2). Liver biopsies were obtained from two of these monkeys and from one monkey with normal levels of RBC arginase activity. Arginase from both groups of animals required Mn²⁺ for maximal enzyme activity and demonstrated a pH optimum of 10.2 in vitro. The activity of arginase in the livers of all three monkeys was 1.1 mmol arginine cleaved/g protein/min. The apparent K _m for arginine of arginase in the livers of the RBC-deficient monkeys was 7.4 and 5.9mm and in the normal monkey was 6.9mm. Similar patterns of heat denaturation were seen at 69 C without Mn²⁺ present and 79 C in the presence of 20mm Mn²⁺. No difference in mobility on either acidic or basic polyacrylamide gels for liver arginase from either RBC-deficient or normal monkeys was found. In addition, liver arginase from all three monkeys reacted similarly with anti-human liver arginase antibody. Liver arginases in RBC-deficient and normal monkeys were identical by ten criteria. These studies do not distinguish among several hypotheses for the genetic determination of arginase in different organs of this species and of man.     

Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured by accelerometer

There are large individual differences in the daily pattern and level of physical activity in humans and other species. As it is becoming apparent that activity plays an integral role in a number of physiological processes including arousal, attention, cardiovascular health and body weight regulation, there is an increased interest in quantifying activity. Nonhuman primates are particularly useful experimental models for such studies in that they exhibit a repertoire of activity more similar to humans than the activity of animals such as rodents and domestic animals. Recent studies measuring activity in nonhuman primates have used omnidirectional accelerometers, often worn on collars; however, the exact behaviors and movements detected by monkeys wearing these devices have not yet been characterized. To test the hypothesis that collar-worn accelerometers primarily detect movements that involve movement of the whole body, 16 adult female rhesus monkeys, housed individually in stainless steel cages, wore loose-fitting collars with an attached small metal box housing an activity monitor (Actical omnidirectional accelerometer; MiniMitter Inc., Bend, OR) and behavior was videotaped. Videotaped behaviors were analyzed by frame-by-frame analysis. There was a significant correlation between total (all) movement revealed by videotape analysis and activity counts detected by the accelerometers (r(s)=0.612, P=0.012), primarily reflecting a strong correlation between whole body movement and activity counts (r(s)=0.647, P=0.007). In contrast, arm movement (r(s)=-0.221, P=0.412) and head/neck movement (r(s)=0.193, P=0.474) were not correlated with activity counts. These findings support the hypothesis that activity monitor placement on a collar allows for effective quantification of whole body movement in monkeys, and indicate that behaviors such as chewing and arm movement do not significantly influence activity recorded by collar-mounted accelerometers.     

Behavioral rhythms in the Nilgiri langur,Presbytis johnii

Eighteen complete daily profiles of 16 behaviors were compiled for three troops of Nilgiri langurs from Periyar Sanctuary in South India. Daily behavioral peaks from these profiles were tested for their associations with each other. Daily rhythms of feeding and resting showed four to eight peaks per day. When all observation days were lumped, however, a bimodal curve resulted as noted by most authors who have studied activity rhythms. The major daily behavioral associations were as follows: (1) feeding occurred during high rates of movement although not during major movement periods; (2) measures of troop movement were interrelated and occurred when troop members were dispersed; (3) movement was related to such active behaviors as whooping displays, coughing, juvenile whining, urinating, and scratching; (4) the above active behaviors showed some positive associations with each other; (5) play, grooming, and scratching showed positive associations with each other; and (6) rest periods were primarily periods of close social contact when grooming occurred and juveniles were with their mothers.     

Induction of diabetes with signs of autoimmunity in primates by the injection of multiple-low-dose streptozotocin

Aim

To develop a preclinical large animal model of autoimmune diabetes to facilitate the translational research of autoimmune diabetes in human.

Materials and methods

Nine young rhesus monkeys received multiple-low-dose (MLD) intravenous injections of streptozotocin for five consecutive days, followed by two additional boosting injections of STZ given 1 week apart. The induction of autoimmune diabetes was evaluated by regular metabolic testing, serological assessment of islet-reactive autoantibodies and histological examination of pancreatic tissues.

Results

Seven of nine treated animals became diabetic with moderate hyperglycemia initially and more severe hyperglycemia thereafter. All diabetic animals exhibited severely impaired glucose tolerance, limited islet function, and required insulin therapy to maintain relatively normal glucose metabolism and healthy status. Serological tests showed that all diabetic monkeys developed autoantibodies specifically against insulin and islet antigens. Furthermore, histological examination of the pancreata from diabetic animals revealed evidence of specific destruction of islet β cells and islets infiltrated with T lymphocytes. Overt and persistent diabetes can be induced in young rhesus monkeys by the injection of MLD-STZ, and autoimmune responses to pancreatic islet cells seem to be involved in the development of glucose intolerance and diabetes.

Conclusion

These data indicate for the first time that autoimmune diabetes can be induced in primates; this may serve as a valuable preclinical model for studying the pathogenesis of and potential therapies for autoimmune diabetes in humans.     

Group composition effects on social behaviour of captive squirrel monkeys (Saimiri sciureus)

Feral and semi-feral squirrel monkeys form sexually segregated subgroups. Observation of social interaction among laboratory animals revealed significant differences in social behaviour as a function of group composition. Females were more active in Unisexual groups. They engaged in more affiliative behaviour and were less often the target of agonistic attack. Adult females with young avoided adult males. ‘Aunts’ and Nulliparous females initially avoided these same males, but later spent over 50% of their time in close proximity to them. Results are discussed in terms of squirrel monkey social ecology, and successful child-rearing.     

An “orientation sphere” visualization for examining animal head movements

1. Animal behavior is elicited, in part, in response to external conditions, but understanding how animals perceive the environment and make the decisions that bring about these behavioral responses is challenging.
2. Animal heads often move during specific behaviors and, additionally, typically have sensory systems (notably vision, smell, and hearing) sampling in defined arcs (normally to the front of their heads). As such, head‐mounted electronic sensors consisting of accelerometers and magnetometers, which can be used to determine the movement and directionality of animal heads (where head “movement” is defined here as changes in heading [azimuth] and/or pitch [elevation angle]), can potentially provide information both on behaviors in general and also clarify which parts of the environment the animals might be prioritizing (“environmental framing”).
3. We propose a new approach to visualize the data of such head‐mounted tags that combines the instantaneous outputs of head heading and pitch in a single intuitive spherical plot. This sphere has magnetic heading denoted by “longitude” position and head pitch by “latitude” on this “orientation sphere” (O‐sphere).
4. We construct the O‐sphere for the head rotations of a number of vertebrates with contrasting body shape and ecology (oryx, sheep, tortoises, and turtles), illustrating various behaviors, including foraging, walking, and environmental scanning. We also propose correcting head orientations for body orientations to highlight specific heading‐independent head rotation, and propose the derivation of O‐sphere‐metrics, such as angular speed across the sphere. This should help identify the functions of various head behaviors.
5. Visualizations of the O‐sphere provide an intuitive representation of animal behavior manifest via head orientation and rotation. This has ramifications for quantifying and understanding behaviors ranging from navigation through vigilance to feeding and, when used in tandem with body movement, should provide an important link between perception of the environment and response to it in free‐ranging animals.

     

Menstrual cycle and some other related aspects of Japanese monkeys (Macaca fuscata)

The menstrual cycle and some other related aspects of Japanese monkeys (Macaca fuscata) were dealt with in this paper. Almost all the monkeys had regular menstrual cycles only in the mating season, and had no menstrual cycles, or only irregular ones, in the non-mating season. The average length of the menstrual cycle in the mating season was 26.3 ±5.4 days. Many monkeys had a tendency to have their own individual and relatively regular cycles. Ninety out of 108 monkeys kept in the air-conditioned quarters for five years showed “periodical changes” essentially coincident with the changes of outdoor season, and this fact suggests that the rhythm of the seasonal change of Japanese monkeys remains for a relatively long period even if the monkeys are kept in air-conditioned quarters where room temperature and lighting are kept constant throughout the year. Vaginal smear, cervical mucus, sexual skin, etc. were observed in relation to ovulation. These characters showed cyclic changes with menstrual cycles in about half of all cases observed, but ovulation occurred even in the cases in which no cyclic change was observed. Therefore, it was not necessarily easy to estimate the ovulation by observing these characters.     

Responses of a transplanted troop of Japanese macaques (Macaca fuscata) to bobcat (Lynx rufus) predation

A series of encounters between a transplanted troop of Japanese monkeys (Macaca fuscata) and one or more bobcats (Lynx rufus) is described. One incident of predation was observed and four additional cases assumed. Reactions of identified individuals and groups of monkeys as well as general troop reactions are noted. The effects of breeding season behavior, troop size, differences in mother care, behavior of the bobcat, and the structure of the south Texas environment are explored. After the observed predation incident, intervention by the researchers affected the behavior of the monkeys and the bobcat, and reduced encounters.     

Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus)

Squirrel monkeys (Saimiri sciureus, Iquitos) were exposed to a sequence of three stresses: A live snake, ether anesthesia, and physical restraint. Plasma cortisol concentrations were determined both following each stress exposure and before and after the sequence of stresses. Dominant males demonstrated lower unstressed plasma cortisol levels than subordinates. Although the form of the relationship between adrenal activity and social dominance differs for the types of stress, dominant animals always show the greatest adrenal reactivity to stress.     

Testing for Links Between Female Urine Odor and Male Sexual Behaviors in Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Urine is involved in sexual communication in New World monkeys and lemurs, but most studies of the role of olfaction in sexual communication in Old World monkeys have focused on vaginal secretions rather than urine. We investigated whether female urine promotes male sexual behaviors (approaches and inspections of genital area) in Japanese macaques (Macaca fuscata). We used a sequential presentation paradigm in behavioral experiments, presenting unfamiliar female urine and control cotton swabs to males living in a social group with cycling females. We tested whether males (N = 3) showed more processing behaviors (licking, sniffing, tasting) toward female urine (22 stimuli per male from prefertile, fertile, and postfertile phases, based on urinary estrone and progesterone conjugate profiles) than control odor (8 stimuli per male). We then compared male sexual behaviors toward resident females pre- and post-exposure to stimuli and in relation to the females’ reproductive status (perifertile, nonfertile, and pregnancy periods, based on fecal estrone and progesterone conjugate profiles). We found that males showed significantly more processing behaviors toward urine stimuli than to controls but that male behavior did not vary across urine samples from prefertile, fertile, and postfertile phases. Exposure to unfamiliar female urine stimuli did not modulate male approaches to and inspections of resident females at any stage of the female reproductive cycle. Although our study is limited by its small sample size, the results suggest that female urine contains compounds that males detect, but we found no evidence that female urine is related to male sexual behaviors.     

Group responses to parturition inMacaca arctoides

The birth of an infant to the highest ranking female in a captive social group of stumptail macaques (Macaca arctoides) is described. Along with certain details of delivery behavior, the responses of group members to the birth are given. The alpha male and two juvenile males were sexually aroused just prior to and during parturition. Adult females paid no special attention to the birth. A subadult nulliparous female and a young adult primiparous female showed interest in the eating of the placenta by the female. The new mother's juvenile son was the monkey closest to her for about two hours after the birth; approaches by other monkeys, especially adult males were avoided. Time of delivery, signs of labor, and the behavior of the mother are also included.     

A field study of the pigtail monkey (Macaca nemestrina)

A field study of the pigtail monkey (Macaca nemestrina) was conducted in Malaysia. An initial six month survey revealed a badly disturbed, diminishing population. Intensive observation required prolonged extensive habituation efforts including a modified form of provisionization and the use of a trained captive pigtail monkey. The pigtail monkey was found to be an arboreal deep forest animal which, nonetheless, came to the ground more often than any other monkey in the forests of Malaya. Responses observed in the natural habitat could not be differentiated from those seen in captive groups; but response frequencies differed. Social patterns observed were similar to those seen in other macaques but differed notably from those seen in sympatric leaf monkeys. Travel patterns, feeding, agonistic responses, sexual behavior, play and other responses are described and discussed.     

Social environment and weather during early life influence gastro-intestinal parasite loads in a group-living mammal

Conditions experienced during early life have been frequently shown to exert long-term consequences on an animal’s fitness. In mammals and birds, the time around and shortly after weaning is one of the crucial periods early in life. However, little is known about how social and abiotic environmental conditions experienced around this time affect fitness-related traits such as endoparasite loads. We studied consequences of social interactions and rainy weather conditions around and after weaning on gastro-intestinal nematode loads in juvenile European rabbits Oryctolagus cuniculus. Infestations with the gastric nematode Graphidium strigosum and with the intestinal nematode Passalurus ambiguus were higher in animals experiencing more rain during early life. This might have been due to the higher persistence of nematodes’ infective stages outside the host body together with the animals’ lower energy allocation for immune defence under more humid and thus energetically challenging conditions. In contrast, infestations with P. ambiguus were lower in animals with more positive social interactions with mother and litter siblings. We propose that social support provided by familiar group members buffered negative stress effects on immune function, lowering endoparasite infestations. This is supported by the negative correlation between positive social behaviour and serum corticosterone concentrations, indicating lower stress in juveniles which integrated more successfully into the social network of their group. In conclusion, the findings offer a pathway showing how differences in the abiotic environment and social life conditions experienced early in life could translate into long-term fitness consequences via the effects on endoparasite loads.     

Learning and perception of oddity problems by lemurs and seven species of monkey

Eight nonhuman primate species were compared in three experiments utilizing the oddity paradigm. The sample included 4 lemurs (Lemur catta), 26 Old World Monkeys (Macaca mulatta, M. nemestrina, M. speciosa, andCercopithecus nictitans) and 21 New World Monkeys (Cebus apella, Lagothrix humboldti andSaimiri sciurea). EveryS was first trained 60 days on “outside oddity” problems. Next,Ss solved “outside” oddity problems constituted from two short and two tall cylinders, and were tested for their perception of oddity withDavis andMcDonald's (1962) technique of varying the height of the centerplaced but nonreinforced stimulus. In the final experiment,Ss were given ambiguous oddity problems that could be solved either for form or color cues, andEs recorded preference. Cebus and woolly monkeys formed oddity learning sets as well as or better than any of the Macaque monkeys, but relatively poor performances were made by squirrel monkeys, spotnose monkeys, and lemurs. Woolly monkeys were outstandingly accurate in their perception of oddity based on changing stimulus height, no other species approaching them in this skill. Old World Monkeys were much more likely than New World Monkeys to use color as a cue.