Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta)

The development of self-biting behavior in captive monkeys is little understood and poses a serious risk to their well-being. Although early rearing conditions may influence the expression of this behavior, not all animals reared under similar conditions self-bite. The purpose of this study was to examine the effects of three rearing conditions on biting behavior and to determine whether early infant behavior can predict later self-biting. The subjects were 370 rhesus macaques born at the National Institutes of Health (NIH) Animal Center between 1994 and 2004. They were reared under three conditions: mother-reared in social groups (n=183), peer-reared in groups of four (n=84), and surrogate-peer-reared (n=103). Significantly more surrogate-peer-reared animals self-bit compared to peer-only or mother-reared animals. There was no sex difference in self-biting, but this result may have been affected by a sex bias in the number of observations. The durations of behaviors exhibited by the surrogate-peer-reared subjects were recorded in 5-min sessions twice a week from 2 to 6 months of age while the animals were in their home cages and play groups. In the play-group situation, surrogate-peer-reared subjects who later self-bit were found to be less social and exhibited less social clinging than those that did not self-bite. Home-cage behavior did not predict later self-biting, but it did change with increasing age: surrogate clinging and self-mouthing decreased, while environmental exploration increased. Our findings suggest that surrogate rearing in combination with lower levels of social contact during play may be risk factors for the later development of self-biting behavior.     

Temperament correlates with training success in adult rhesus macaques

In recent years there has been a marked increase in awareness of issues involving the psychological well-being of nonhuman primates (NHPs) used in biomedical research. As a result, many facilities are starting to train primates to voluntarily cooperate with veterinary, husbandry, and research procedures, such as remaining still for blood draws or injections. Such training generally reduces the stress associated with these procedures, resulting in calmer animals and, ultimately, better research models. However, such training requires great investments in time, and there can be vast individual differences in training success. Some animals learn tasks quickly, while others make slower progress in training. In this study, we examined whether temperament, as measured by response to a novel food object, correlated with the amount of time it took to train 20 adult female rhesus macaques to perform a simple task. The monkeys were categorized as "exploratory" (i.e., inspected a novel object placed in the home cage within 10 sec), "moderate" (i.e., inspected the object within 10-180 sec), or "inhibited" (i.e., did not inspect the object within 3 min). We utilized positive reinforcement techniques to train the monkeys to touch a target (PVC pipe shaped like an elbow) hung on their cage. Temperament correlated with training success in this study (Pearson chi2=7.22, df=2, P=0.03). We easily trained over 75% of the animals that inspected the novel food (i.e., exploratory or moderate individuals) to touch the target. However, only 22% of the inhibited monkeys performed the task. By knowing which animals may not respond to conventional training methods, we may be able to develop alternate training techniques to address their specific needs. In addition, these results will allow us to screen monkeys to be assigned to research projects in which they will be trained, with the goal of obtaining the best candidates for those studies.     

Reactions of nuclear-family–reared rhesus macaques to the births of younger siblings

A group of juvenile rhesus macaques (Macaca mulatta) living in a nuclear-family laboratory environment was studied to determine their responses to the births of siblings. The frequencies of interactions with family members (mothers, fathers, and new siblings) and nonfamily (peers, unrelated infants, and unrelated adults) were studied over both the year preceding and the year following sibling birth. The frequencies of specific behaviors in each of those interactions and the frequencies of interactions in each area of the nuclear-family unit (home cage, play area, or other families' cage) were also examined. After new siblings arrived, several measures of interactions with mothers, fathers, and new siblings increased significantly; by contrast interactions with peers decreased substantially over the post-birth year. Although the frequency of interactions in home cages remained stable over the 2-year period, interactions outside of the subjects' home cages decreased significantly after siblings were born. An additional subject group whose mothers became pregnant but failed to deliver viable offspring showed no significant changes in total levels of interactions with peers; they did, however, exhibit increases in some interactions with unrelated infants and adults. Female juveniles interacted with new siblings significantly more often than did males when siblings were less than 6 months old, but as siblings grew older (6–12 months), females' levels of interaction with them fell to a level equal to that of males. In the nuclear-family social structure, the birth of a sibling resulted in an increased emphasis on family interactions at the expense of peer interactions.     

Social interactions among female rhesus macaques (Macaca mulatta) during the nonbreeding season: Responses to the introduction of males

When rhesus monkeys are observed in social groups during the breeding season, increases in interfemale aggression coincide with midcycle increases in sexual activity between males and females. However, some investigators have suggested that both aggressive and affiliative interactions between females are influenced by the presence or absence of males, irrespective of menstrual cycle stage. In the present study, social interactions among members of a captive group of rhesus females were measured during the non-breeding season in response to the introduction of rhesus males. Ovariectomized rhesus females (estrogen-treated or untreated) served as stimulus controls. Tests with males were characterized by significantly decreased interfemale proximity and grooming and significantly increased aggression from that seen in tests with stimulus females or in the absence of stimulus animals. Only interfemale proximity declined significantly during stimulus female tests, but results suggest that this may merely reflect a decline in this behavior that occurs across the course of the day. Estrogen treatment did not alter either the aggressive or affiliative behavior of stimulus females or group female response to stimulus females. The possibility is discussed that changes in interfemale interactions during tests with males reflect female interest in interacting with the male, particularly under social conditions that may limit such interactions.     

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta)

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.     

Positive reinforcement training in rhesus macaques—training progress as a result of training frequency

Positive reinforcement training (PRT) efficiency was examined as a function of training frequency in 33 pair‐ or triple‐housed female rhesus macaques. The animals were trained three times a week, once a day or twice a day, using PRT and a clicker as a secondary reinforcer. All animals were trained on 30 sessions, with an average of 5 min per training session per animal. The behaviors, trained in succession, were Targeting (reliably touching and following a Target); Collaborating (dominant animals allowing subordinates to train while stationing); Box‐training (accepting being enclosed in a small compartment while responding to Target training) and initial Injection training. Fulfilled criteria for Targeting were obtained in 32/33 animals in a median of nine training sessions. Collaboration was obtained in 27/33 animals in a median of 15 training sessions. However, only four animals completed Box‐training during the 30 training sessions and started Injection training. When comparing training success in terms of number of training sessions, training twice a day was less efficient than the other two treatments. In terms of daily progress, our results suggest that from a management perspective, daily training is more conducive to quick training success than thrice weekly training. In addition, in this study no further advantages could be gained from training twice a day. Am. J. Primatol. 71:373–379, 2009. © 2009 Wiley‐Liss, Inc.     

The positive aspects of correct negative reinforcement

Abstract

In the scheme of contemporary animal training, horse training is virtually unique because it relies on negative reinforcement (NR) rather than positive reinforcement (PR). Furthermore, horse trainers are largely unaware that they are using NR in training. Instead, they believe in the benevolent nature of the horse and see their task in training as one of improving the balance and gymnastic ability of the horse—outcomes that emerge when the rider is similarly properly balanced. Under these conditions, it is claimed the willing horse will perform its required maneuvers. These beliefs may be associated with several welfare issues and indicate areas requiring future research: 1. The absence of release of pressure, the release of pressure at the wrong times, the use of opposing pressures simultaneously and the absence of shaping procedures are central to the development of acute and chronic stress responses in horses.

2. Resultant conflict behaviors contribute to equine wastage statistics and include behaviors that are dangerous to horses and humans.

3. There is a need for research into the mechanics of NR because it is poorly researched compared to PR.

4. When NR responses are installed correctly, only mild pressures need to be used, and results are obtained in few trials.

5. Many qualified animal trainers misunderstand NR and confuse it with punishment. They believe that PR has positive welfare implications and thus NR being “negative,” has negative welfare implications. So there is a need for horse trainers to understand learning theory and the principles that surround NR.

6. Horse trainers are isolated from advances in animal training. Therefore they increasingly seek knowledge and solutions from the growing number of “horse whisperers” and unqualified “horse psychologists.” This is potentially detrimental for the welfare of the horse and the need is urgent for universities throughout the world to become the knowledge bases for equitation science.

     

Relation between the dominance rank of female rhesus monkeys and their access to males

Systematic observations were made on 12 measures of the sexual, aggressive, and social interactions of 24 male–female pairs of rhesus monkeys in six social groups, each consisting of one male and four ovariectomized females tested in a large room. Each female in a group was treated in turn first with estradiol alone and then with estradiol and progesterone in combination. When hormone-treated, the female was also observed during pair tests with the male in the same large observation room (four males, eight females, 240 group tests, 240 pair tests). The dominance ranks of females during group tests were determined post hoc by means of the dominance index [Zumpe & Michael, American Journal of Primatology 10:291–300, 1986]. In all six groups, the most dominant female virtually monopolized the male, and the subordinate females' interactions with the male, assessed during pair tests, were almost completely suppressed during group tests. This “dominant female effect” was a robust phenomenon that depended solely on female dominance rank. It was independent of the identity and hormonal status of females and of the social preferences of males as expressed in pair tests. These findings demonstrate the existence of female mate competition in an Old World primate.     

Influence of regional crossbreeding between rhesus macaques on the rate of weight gain of their offspring

To evaluate potential heterosis resulting from breeding between rhesus macaques of Chinese and Indian origin in a captive social group, the rates of weight gain of Indian (nonhybrid) rhesus monkeys were compared with those of their hybrid (half Chinese/half Indian) peers. The coefficients for the linear regression of age on weight were estimated for each animal for each exact age between 1 and 4, when that regression is strictly linear, at which he/she lived in the group. The average rates of weight gain of hybrids and nonhybrids were compared using the t statistic. Both male and female hybrids exhibited statistically significantly higher rates of weight gain than their nonhybrid peers before, but not after, age 4. No evidence could be found that either hybrid status or rate of weight gain increases fitness, at least under captive conditions. © 1994 Wiley-Liss, Inc.     

Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors

Upon discovering food, free-living rhesus macaques (Macaca mulatta)on the island of Cayo Santiago, Puerto Rico, produce a complexof vocal signals consisting of five acoustically distinguishablecalls. This report examines the socioecological factors elicitingcall production and the information protentially conveyed toothers. The primary contexts for three vocalizations ("warbles," "harmonicarches, " and "chirps") are encounters with rareand highly preferred foods (e.g., coconut). Two other vocalizations("coos" and "grunts") are produced both in food (primarily provisionedchow) and in nonfood contexts, such as during mother-infantseparation and grooming interactions. Grunts given upon encounteringfood are acoustically distinct from those given in nonfood contexts.In contrast, coos associated with food are statistically indistinguishablefrom coos given in other contexts. When conspecitics hear thesefood-associated calls, they typically approach the caller. Coosare less likely to lead to approach than other food-associatedcalls, Results from all-day follows on adult males and adultfemales reveal that changes in hunger level influence call ratebut not call type; the different call types are produced throughoutthe day. We infer that the structure of food-associated callsprovides information about the quality of the food discovered,whereas call rate conveys information about the relative hungerlevel of the caller. In this population, adult males give fewerfood-associated calls than adult females. In addition, femaleswithin large matrilines call more than females within smallermatrilines, and males who are resident in a group are more vocalthan peripheral males.     

A test of the generalizability of the interval scale developed for social behavior of rhesus monkeys

An interval scale of behavior would be useful in the study of social relations because it would allow the whole behavioral repertory to be used simultaneously and would allow greater flexibility in statistical manipulation. Maxim has developed such a scale using isolated dyads of unfamiliar monkeys. The typical social environment of monkeys, however, consists of familiar monkeys in mixed age and sex groups. This study replicates Maxim's procedure and tests the applicability of a scale developed with isolated dyads to groups of familiar monkeys. The scale developed here differed substantially from Maxim's. Behavior of monkeys in these groups was much more variable than behavior of monkeys in Maxim's isolated dyads. Behaviors at the extremes of the scale were similarly arranged in both scales, but behaviors in the central region were more labile and disordered. Distances between behaviors at the extreme of this scale were significantly larger than those in the central region whereas there were no differences in Maxim's scale. While some of these differences may be accounted for by group size and familiarity, several difficulties remain. Some behaviors may change meaning across different contexts and social relationships. The generalizability of these scales, therefore, may be limited to the behavior of groups of similar composition and familiarity.     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

The formal hierarchy of rhesus macaques: An investigation of the bared-teeth display

Teeth-baring in a large captive rhesus monkey group (Macaca mulatta) was observed over a 30-month period. Its directional consistency among adults was significantly higher than that of aggression. The unidirectionality was so extreme that the facial display must be seen as a formal status indicator; ie, a signal of which the direction is independent of short-term contextual variation. As such, it seems adapted for communication about the state of the relationship. Formal dominance relationships among adults could be arranged in a hierarchy which approached perfect linearity. Focal observations demonstrated that teeth-baring was associated with withdrawal. It was uncommon among foraging monkeys, perhaps because dominant animals paid less attention to their subordinates in this context. The speed of rank acquisition by young females, in terms of received teeth-baring, was highest among peers and lowest against the group's old matriarchs. The age at which dominance over unrelated adult females was achieved correlated negatively with the amount of affiliative contact with these females. This translates into a positive correlation between bonding and rank establishment, indicating that dominance processes may be indistinguishable from social integration.     

Demodex spp. in the hair follicles of rhesus macaques (Macaca mulatta)

The perineal or perineal and facial skin were evaluated on 53 rhesus macaques as part of a necropsy protocol. Microscopic evaluation of H & E stained skin sections revealed 19 animals positive for Demodex spp. Mites were seen within all portions of the hair follicles. Infestation varied from minimal to severe. Mites were found in macaques of all ages and in both sexes. Reaction to the mites ranged from no reaction, to minimal follicular epidermal hyperplasia to furunculosis. Immune status of the animal did not determine infestation but immune compromised macaques had more severe lesions. This is the first known report of Demodex spp. in rhesus macaques.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosures

Positive reinforcement techniques were applied to train groups of chimpanzees to move voluntarily into the indoor portions of their enclosures at the request of trainers and to be briefly restricted to those areas. Subjects were 66 members of eight social groups, including 44 adults (14 males, 30 females), and 22 immatures (eight males, 14 females). Performance of individual animals was recorded during four experimental phases of the project: baseline, initial training, maintenance of reliable performance, and transfer of responsibility for training from the original trainers to others on staff. A mean of 16.1 training sessions was required to reach reliable performance, defined as the subjects' complying with 90% of the requests to move indoors. Analyses of variance indicated that chimpanzee compliance was significantly increased after training. Females required significantly fewer training sessions to reach reliable performance than did males. Adult males showed the lowest level of compliance in each experimental phase. Overall, compliance was not affected by the transfer of responsibility for the procedure from the original trainer to other staff, although there was evidence of a temporary and small decrement in performance immediately following transfer. These findings indicate that training can improve the voluntary movement of captive chimpanzees. They also demonstrate that animal training can be objectively evaluated using systematic study design, data collection, and statistical analysis of data. Zoo Biol 17:333–341, 1998. © 1998 Wiley-Liss, Inc.     

环境和社会因素对喀斯特石山猕猴日活动节律和活动时间分配的影响

2007年9月至2008年8月,以广西弄岗国家级自然保护区内的一大群野生猕猴为研究对象进行连续的跟踪观察,采用瞬时扫描取样法收集其食物组成、活动节律和活动时间分配的数据,旨在探讨影响石山猕猴活动节律及活动时间分配的环境和社会因素。结果表明：研究猴群的日活动节律表现为上午和下午的觅食高峰以及中午的休息高峰,这与白天温度和日照强度的变化有关。日活动时间分配中,休息42.1%,移动34.5%,觅食15.1%,玩耍2.0%,理毛5.2%,其他行为1.3%。猴群依据食物的变化调整活动时间分配,其中用于移动的时间与食物中果实的比例成显著的正相关性。不同性别年龄组个体的活动时间分配表现出显著差异,主要表现为成年雄性花费更多的时间休息,而成年雌性花费更多的时间觅食和社会性理毛,未成年个体则花费更多的时间玩耍。与同域分布的小群猕猴相比,本研究群花费更多的时间休息,较少的时间觅食。这些差异可能与盗食农作物有关。     

The hemogram,serum biochemistry,and electrolyte profile of the free-ranging Cayo Santiago rhesus macaques (Macaca mulatta)

Sixty-four male and 33 female free-ranging rhesus monkeys (Macaca mulatta) from one of six social groups on the island of Cayo Santiago, Puerto Rico, were surveyed to establish normal values for the hemogram and serum biochemical and electrolytes for the colony. Mean values (± 1 SD) are reported by sex for each of three age groups (2–3, 4–9 and ≥ 10 years). All adult females (≥ 4 years) were pregnant. There were significant differences for a number of variables compared to the range reported in the existing literature, and among the age and sex groups in the sampled population.     

Adoption by captive parturient rhesus macaques: Biological vs. adopted infants and the cost of being a “twin” and rearing “twins”

Four rhesus macaque (Macaca mulatta) mothers each spontaneously adopted and reared an abandoned, unrelated neonate in addition to their own neonate. Data on relative time spent in maternal contact and who maintained proximity were collected for the biological and adopted “twins” and singleton control infants using focal animal sampling. Infant weight gain and the subsequent conception history for each mother were obtained for the following year. Biological infants spent more time in maternal contact than their adopted “twin” siblings. When in contact with their mothers, biological “twins” spent more time in the ventro-ventral position and more ventral time alone than adoptees. Mothers initiated more contacts with their biological infants than their adopted infants, suggesting these differences may be due to differential maternal behavior. “Twins” gained weight at a slower rate than singletons, and mothers rearing “twins” produced significantly fewer offspring the following season. Am. J. Primatol. 43:259–264, 1997. © 1997 Wiley-Liss, Inc.