Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (Gorilla gorilla)

To evaluate whether observed cycles in proceptive behavior in aging lowland gorilla females (age 40+) at Brookfield Zoo were driven by ovarian activity, we compared monthly behavioral data to estradiol and progestogen cycles based on fecal hormone assessments. Progestogen peaks showed regularity and close coincidence with monthly sexual behaviors. Estradiol was more variable. Progestogen peaks varied between 22+/-5 days for the control female (29 years old), to 24+/-2.5 and 29+/-8 for the two aged subjects. In the first aged female, which was housed with other females and a silverback, the high degree of cyclicity in sexual behavior, regularity of progestogen cycles, and close concordance between hormonal cycling and sexual behavior strongly compared to patterns found (in this and other studies) in gorilla females <35 years old. Cyclical progestogen peaks were longer and more variable in the second aged female-perhaps because she lacked the social mediation of other females or a male. For husbandry reasons she is not housed with the gorilla group, behavioral data were not collected from her. The value of our longitudinal study is in obtaining reproductive profiles of primate females that are approaching maximum lifespan. This pilot study is part of a larger research project on reproductive senescence that will include other captive females >35 years old, a population that is rapidly increasing in North American zoos as gorillas continue to age.     

A case study of primiparous maternal and infant gorilla (Gorilla gorilla gorilla) behavior

A primiparous mother and her infant were subjects of a longitudinal behavioral study at Lincoln Park Zoo in Chicago, Illinois. From November 1998 to November 1999, we collected a total of 100 hr of focal nonhuman animal instantaneous point sampling and all occurrence data on the mother and her infant. After 8 months, we introduced the 4-member focal group to an 8-member gorilla group, thus providing an opportunity to study the effect of the introduction on mother-infant behavior. Overall, time the pair spent physically apart was notably high with contact and proximate scores steadily decreasing over time. The infant was largely responsible for maintaining social proximity, rarely leaving the mother and frequently approaching her. In contrast, the mother left the infant frequently and approached the infant minimally. Maternal affiliative and nonaffiliative behaviors fluctuated throughout the study. Over time, both decreased. Despite a precarious maternal relationship, infant developmental trends were typical for captive gorillas. The results of this study suggest that allowing flexibility in judging maternal conduct can be of benefit to successful gorilla husbandry.     

A Case Study of Primiparous Maternal and Infant Gorilla (Gorilla gorilla gorilla) Behavior

A primiparous mother and her infant were subjects of a longitudinal behavioral study at Lincoln Park Zoo in Chicago, Illinois. From November 1998 to November 1999, we collected a total of 100 hr of focal nonhuman animal instantaneous point sampling and all occurrence data on the mother and her infant. After 8 months, we introduced the 4-member focal group to an 8-member gorilla group, thus providing an opportunity to study the effect of the introduction on mother-infant behavior. Overall, time the pair spent physically apart was notably high with contact and proximate scores steadily decreasing over time. The infant was largely responsible for maintaining social proximity, rarely leaving the mother and frequently approaching her. In contrast, the mother left the infant frequently and approached the infant minimally. Maternal affiliative and nonaffiliative behaviors fluctuated throughout the study. Over time, both decreased. Despite a precarious maternal relationship, infant developmental trends were typical for captive gorillas. The results of this study suggest that allowing flexibility in judging maternal conduct can be of benefit to successful gorilla husbandry.     

Evaluating changes in salivary oxytocin and cortisol following positive reinforcement training in two adult male western lowland gorillas (Gorilla gorilla gorilla)

Positive reinforcement training (PRT) is associated with increases in species-typical behavior and decreases in stereotypic and abnormal behavior in participating animals. Physiological changes following PRT, for example, increases in oxytocin (OXT) and/or decreases in cortisol (CORT), may facilitate these behavioral changes. This study evaluated salivary OXT and salivary CORT concentrations in two adult male western lowland gorillas (Gorilla gorilla gorilla) following PRT with their primary animal care staff. Following PRT, no change in OXT was observed. CORT decreased in one subject following PRT. Changes in endogenous OXT are related to affiliative interactions and interact with strongly bonded conspecifics. PRT may not activate the oxytocinergic system because PRT is not a species-specific affiliative interaction and/or animal care staff are not viewed as conspecifics. Regardless, PRT may still be viewed as a positive interaction resulting in stress reduction via a decrease in CORT. Relationships are unique, thus these results only apply to these two gorillas and one animal caregiver. Larger population-level studies are needed to understand overall trends in human–animal interactions, and ultimately human–animal relationships. Further evaluation of physiological changes following human–animal interactions should be informative for understanding the human–animal relationship in zoos.     

Effects of Temporal Sampling Patterns of All-occurrence Recording in Behavioural Studies: Many Short Sampling Periods Are Better than a Few Long Ones

All-occurrence recording is generally thought to yield unbiased results. However, its accuracy and power to detect real effects may depend on the temporal patterning of the observation periods. Although several studies evaluated the suitability of time-sampling methods (one-zero and instantaneous sampling), there has not been an evaluation of various temporal patterns of the ‘all-occurrence’ method to date. Here we present an empirical comparison of time-sampling and all-occurrence recording methods, based on a large data set, with special reference to various temporal patterns of all-occurrence recording. The three different sampling methods were imposed on raw data protocols. The scores, obtained by the use of each method and temporal pattern, were compared with true values from the corresponding continuous video recordings. The accuracy and power of each method was estimated by comparison of medians and magnitudes of effect (r_m), respectively. We were able to confirm results of earlier studies on the suitability of time-sampling methods (one-zero and instantaneous sampling), but we found that different temporal patterns of all-occurrence sampling yielded magnitudes of effect that differed from true value magnitudes. We conclude that behavioural studies may reveal different results, even when all conditions are the same, only because of power differences of different temporal pattern of the observation periods, for example 1 × 15 min versus 15 × 1 min. Recommendations are made about appropriate application of methods.     

A preliminary behavioral comparison of two captive all-male gorilla groups

Gorillas live in polygamous harem groups, generally composed of one male, several adult females, and their offspring. With an equal numbers of male and female gorillas born in captivity, however, housing gorillas in social breeding units inevitably means that some males will not have access to female social partners. Thus, the future of the captive gorilla population depends on the collective ability of zoos to house equal numbers of males and females. This study examined the behavioral profiles of two all-male groups of captive lowland gorillas (Gorilla gorilla gorilla) to provide information on this type of housing situation. One group consisted of three subadult individuals, while the other consisted of two subadults and a silverback. Data were collected during two 6-month intervals, for a total of 284 hr. The behavioral profiles of the animals were stable over the course of the study but proximity patterns changed. Differences in feeding, solitary play, and object-directed behavior were found between groups, while no significant differences were observed in affiliative or agonistic social behavior. At both institutions, group cohesion appeared to be high, particularly between subadults; these individuals spent approximately 10% of their time engaging in social behavior and 25-50% of their time in close proximity (within 5 m). However, the Zoo Atlanta males spent significantly more time within 1 m and 5 m of each other than the Santa Barbara males, which may reflect a higher level of cohesiveness among members of the Zoo Atlanta group. The behavioral profiles of the animals in this study were similar to those found in bachelor groups of wild mountain gorillas. One notable exception was the absence of homosexual behavior between the silverback and subadults in Santa Barbara and the low frequency of this behavior between subadults in both groups. Although more longitudinal data are needed, these data suggest that all-male groups can be a feasible housing strategy for males at certain periods of their life span. Zoo Biol 20:27-40, 2001. Copyright 2001 Wiley-Liss, Inc.     

Behavioral effects of changing group membership among captive lowland gorillas

Group membership was modified among 4 gorilla groups at Zoo Atlanta in an attempt to increase compatibility and sexual behavior. The modifications ultimately moved 7 adult females among the groups. The moves were made by individually introducing the new group members to the old members, resulting in 18 total introductions. Several individual and social behaviors differed in the two conditions. The most obvious change was a temporary increase in aggressive display behaviors, as well as an increase in contact and social examination, in the postmovement condition. Additionally, the individual behaviors of travelling and eating increased after the introductions, while resting decreased. Other self-maintenance behaviors did not change. Finally, there was an increase in time mothers and offspring spent closer to one another following the moves. Previous research and anecdotal evidence suggest that gorillas respond to changes in group membership with aggression; these data support and extend those data to different age/sex groups, postmovement trends in behavior, and other aspects of gorilla behavior. © 1996 Wiley-Liss, Inc.     

神农架自然保护区川金丝猴投食群友好行为的初步观察

为探讨人工补食条件下川金丝猴(Rhinopithecus roxellana)的友好行为因补食产生的影响,2007年1～9月,采用行为取样法、扫描取样法和全事件记录法对湖北神农架自然保护区大龙潭投食猴群的友好行为进行了观察.共记录到11种友好行为,发生频次居前的是理毛、张嘴、拥抱、游戏、趋近.友好行为的发起者和承受者在性别间差异均不显著,但在年龄间差异均显著.在一雄多雌单元内发起者按次数多少为成年、少年、青年、亚成年猴,承受者的顺序亦如此.在全雄单元内发起者按次数多少为成年、少年、亚成年、青年猴,承受者的顺序亦如此.友好行为在单元内和单元间差异显著,单元内多于单元间.这在一定程度上说明川金丝猴社会单元内个体间的关系紧密,单元间的关系相对疏远.友好行为在繁殖和非繁殖季节差异不显著.     

Sexual behavior in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition

Previous research in gorillas suggests that females engage in post‐conception mating as a form of sexual competition designed to improve their own reproductive success. This study focused on sexual behaviors in a newly formed group of western lowland gorillas (Gorilla gorilla gorilla) housed at Zoo Atlanta. All females engaged in mating outside their conceptive periods, although there was individual variation in the frequency of the behavior. An analysis of the presence/absence of sexual behavior found females, regardless of reproductive condition, were more likely to engage in sexual behavior on days when other females were sexually active. On these “co‐occurrence” days, females were significantly more likely to solicit the silverback, but copulations did not differ from expectation. The results find further evidence for sexual competition among female gorillas and suggest that this may occur throughout their reproductive cycle rather than only during pregnancy. Am. J. Primatol. 71:587–593, 2009. © 2009 Wiley‐Liss, Inc.     

Methods of estrus detection and correlates of the reproductive cycle in the sun bear (Helarctos malayanus)

The objective was to explore multiple methods for detecting and characterizing the reproductive cycle of the sun bear (Helarctos malayanus). Thirteen H. m. euryspilus females, loaned from the Malaysian government to US zoos, were used. Fecal metabolite concentrations of estrogen and progesterone were compared to vaginal cytology, changes in genital appearance, and behavior (videotapes and zookeeper observations). Cytology and video behavior were characterized during five hormonally defined states: high, low, and baseline progesterone, estrus, and high estrogen. Among states, there were significant differences in cytology and behavior. Sexual, affiliative, and stereotypic behaviors were highest during estrus, whereas affiliative and social behaviors were lowest during high progesterone. In this captive breeding population, 30.8% of females cycled two or three times a year, 30.8% cycled once a year, and 38.5% did not cycle during this study. Inter-estrus intervals were (mean ± SEM) 115.7 ± 6.3 d (range, 101-131). Spearman rank correlations were significant between both ordinal sexual and affiliative behaviors and vulva swelling and color. Sexual behavior was significantly positively correlated with superficial and keratinized cells, but negatively correlated with parabasal and basophilic cells in cycling females (opposite pattern for appetitive behavior). In conclusion, data for cytology, vulva changes and behavior were consistent with, and complementary to, hormonal data; collectively, they delineated estrus and identified specific reproductive types.     

Integration of New Males into Four Social Groups of Tufted Capuchins (Cebus apella)

We examined how aggressive, affiliative, and sexual behavior function to integrate male capuchins (Cebus apella) into a new social group. Nine males were exchanged among four social groups. We performed instantaneous scans and all-occurrence sampling during baseline, introduction, and follow-up periods. The study included three different introduction situations: 1) males familiar to one another were introduced to a group with no other adult male, 2) males unfamiliar to one another were introduced to a group with no other adult male, and 3) males familiar to one another were introduced to a group with an existing elderly, resident male. Severe aggression occurred in situations 2 and 3, but the introductions were peaceful in situation 1. In all cases proceptive females were among the first individuals to affiliate with the males, and males did not appear to compete for access to proceptive females. Following their period of proceptivity, the females that had cycled remained preferred social partners for the males. Immature animals also quickly affiliated with the new males, and the males tolerated the attention from immatures. Affiliative relationships between the males and nonproceptive females developed slowly, and while male-female aggression was mild, aggression among adult males (familiar and unfamiliar) had the potential to be severe.     

A ten-month study of endogenous testosterone levels and behaviour in outdoor-living female rhesus monkeys (Macaca mulatta)

Endogenous testosterone levels were measured in association with sexual, aggressive, and social/affiliative behaviors in 11 outdoor-housed female rhesus monkeys over a ten-month period. Several behaviors (sex directed toward the male, sex received from the male, aggression directed toward the male, submission directed toward the male, submission directed toward the female, and groom another female) were significantly (p<0.05) positively correlated with testosterone in from one to five females. No trends were strong enough across all females to suggest that any of these correlations have species-wide significance. Factor analysis revealed clearcut clusters of behaviors, but elevations in testosterone were not strongly associated with any of these clusters. It is concluded that endogenous testosterone levels have little measurable effect on overt behavior in female rhesus monkeys.     

Physical and activity changes associated with pregnancy in captive lowland gorillas (Gorilla gorilla gorilla)

The physical appearance and the behavior of five lowland gorilla females at two zoos were recorded before and during 14 pregnancies. Whereas only the quality of changes associated with pregnancy had been described previously, in this study the behavior of the females was recorded quantitatively and evaluated statistically. All females at Stuttgart showed distention of the abdomen three to four months before delivery and development of the breasts a few weeks before parturition. Milk was produced by the third month in one case, and in the sixth month or later in the others, sometimes after delivery. The female at Frankfurt stopped social play seven days after conception; the Stuttgart females, in general, stopped, in the first weeks of pregnancy. Social activity and locomotion decreased considerably within the first three months in all females and were significantly different between the pregnant and the nonpregnant state in all the Stuttgart females. In this study, as in others in the literature, behavioral changes were much more reliable signs of pregnancy than were physical changes. Thus the quantitative results confirm those obtained solely by qualitative observation.     

Characterizing the behavior and reproductive biology of zoo-housed Sichuan takin (Budorcas taxicolor tibetana) using non-invasive techniques

The Sichuan takin (takin; Budorcas taxicolor tibetana) is distributed in the Gansu and Sichuan providences of southern China and along eastern Tibet. Because of their ecology, few data on takin reproductive biology exist, with the exception of its mating season in the Sichuan province, which occurs from July through August. Therefore, the objectives were to: 1) characterize reproductive hormones in zoo-housed male and female takin, including pregnancy in the female, using non-invasive fecal steroid hormonal monitoring; 2) characterize behaviors of zoo-housed takin, emphasizing reproductive behaviors and activity budget; and 3) assess the influence of season on births in North America and reproductive hormonal and behavioral activity. Fecal samples were collected 3 to 5 times per week from two adult males and three adult females. Extracted hormones were analyzed using an enzyme immunoassay for progestagen and androgen concentrations. Behavioral observations were collected for 2 yrs using an ethogram. In this study, season affected reproduction, specifically birth occurrences, reproductive cyclicity in females and androgen production in males. The duration of the estrous cycle was approximately 35 d and cycles occurred June through December. Androgen concentrations peaked in May through August. Season did not influence behavior; however, age and sex may affect some behaviors, including activity level, foraging and drinking, social affiliative behavior, and visibility from the visitor's viewpoint. In conclusion, fecal hormonal and behavioral analyses can provide information for management and conservation of this herd species.     

Effects of reproductive state on vocalizations in squirrel monkeys (Saimiri sciureus)

Vocalizations and behavior of a group of 6 squirrel monkeys, 2 males and 4 females, were recorded during the nonbreeding and breeding seasons. Behavioral and physical criteria were used to determine the presence of estrus. During the breeding season the types of vocalizations uttered by estrous females changed, and the adult male increased his rate of vocalizing. Err vocalizations by estrous females were associated with increased following and initiation of affiliative behavior with the adult male, and may have functioned to facilitate these interactions. Errs appeared to be related to changes in female reproductive state rather than to the behavior of others. The adult male increased vocalizations associated with sexual and aggressive behavior (squeals and cackles), primarily in response to the estrous females' persistent initiation of interactions with him. We concluded that certain vocalizations in Saimiri reflected changes in the reproductive state of males and females, and functioned to mediate changes in social bonding during the breeding season.     

Relative growth,ontogeny, and sexual dimorphism in gorilla(Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological considerations

Gorillas are the largest and among the most sexually dimorphic of all extant primates. While gorillas have been incorporated in broad-level comparisons among large-bodied hominoids or in studies of the African apes, comparisons between gorilla subspecies have been rare. During the past decade, however, behavioral, morphological, and molecular data from a number of studies have indicated that the western lowland (Gorilla gorilla gorilla) and eastern mountain (Gorilla gorilla beringei) subspecies differ to a greater extent than has been previously believed. In this study I compare patterns of relative growth of the postcranial skeleton to evaluate whether differences between subspecies result from the differential extension of common patterns of relative growth. In addition, patterns of ontogeny and sexual dimorphism are also examined. Linear skeletal dimensions and skeletal weight were obtained for ontogenetic series of male and female G.g. gorilla (n = 315) and G.g. beringei (n = 38). Bivariate and multivariate methods of analysis were used to test for differences in patterns of relative growth, ontogeny, and sexual dimorphism between sexes of each subspecies and in same-sex comparisons between subspecies. Results indicate males and females of both subspecies are ontogenetically scaled for postcranial proportions and that females undergo an earlier skeletal growth spurt compared to males. However, results also indicate that the onset of the female growth spurt occurs at different dental stages in lowland and mountain gorillas and that mountain gorillas may be characterized by higher rates of growth. Finally, data demonstrate lowland and mountain gorilla females do not differ significantly in adult body size, but mountain gorilla males are significantly larger than lowland gorilla males, suggesting mountain gorillas are characterized by a higher degree of sexual dimorphism in body size. Thus, although lowland and mountain gorillas do not appear to have evolved novel adaptations of the postcranium which correlate with differences in locomotor behavior, the present investigation establishes subspecies differences in ontogeny and sexual dimorphism which may be linked with ecological variation. Specifically, these findings are evaluated in the context of risk aversion models which predict higher growth rates and increased levels of sexual dimorphism in extreme folivores. Am. J. Primatol. 43:1–31, 1997. © 1997 Wiley-Liss, Inc.     

A preliminary study of selective visual attention in female mountain gorillas (Gorilla gorilla beringei)

Visually attending to conspecifics can give group-living primates important ecological information, help them to anticipate the behavior of others and to regulate interactions with them, and provide other valuable social information. Variation in the importance and quality of social relationships should influence the way individuals selectively attend to fellow group members. Preliminary data on visual monitoring of conspecifics by wild female mountain gorillas (Gorilla gorilla beringei) show that selective attention mirrors variation in social relationships. Social bonds between males and females are central to gorilla society; correspondingly, females are more likely to stop feeding, and focus their attention on males who walk into view than on females, especially when males give dislays. Females are more likely to focus on other females with whom they have antagonistic relationships than those (mostly close relatives) with whom they have affiliative, cooperative ones. Further research on the context and consequences of visual monitoring could help to address questions about the regulation of social relationships and about social cognition in gorillas.     

Male chimpanzee behavior in relation to female ano-genital swelling

This study examined the relationships between male agonistic, affiliative, and sexual behaviors and female estrus condition in captive adolescent and young-adult chimpanzees (Pan troglodytes). Data on agonistic, affiliative, and sexual behaviors of 11 males living in three social groups were collected during daily 45 minute observations over a 5 month period. Female estrus condition was assessed daily using the relative size of the female's ano-genital swelling. It was hypothesized that the presence of maximally tumescent females would generate conflicts between males, so an increase in inter-male agonism was predicted. Males exhibited higher rates of agonism toward other males when at least one female in the group was maximally tumescent. Male affiliative behavior directed toward other males and social play with males were affected by the presence and number of maximally tumescent females. Male sexual behavior increased when maximally tumescent females were present.     

Female-female mounting among goats stimulates sexual performance in males

The hypothesis that female-female mounting is proceptivity in goats, in that male goats are aroused by the visual cues of this mounting behavior, was tested. Once a week, male goats were randomly selected and placed in a test pen in which they were allowed to observe one of six selected social or sexual stimulus conditions. The stimulus conditions were one familiar male with two estrous females (MEE); three estrous females that displayed female-female mounting (E(m)); three estrous females that did not mount (E(nm)); three non-estrous females (N(E)); three familiar males (M); and no animals in the pen (Empty). After 10 min, the stimulus animals were removed, and an estrous female was placed in the test pen with the male for a 20-min sexual performance test. During sexual performance tests, the frequencies and latencies of all sexual behaviors were recorded. This procedure was repeated so all males (n = 6) were tested once each test day, and all the stimulus conditions were presented each test day. This was repeated weekly until all males had been exposed to each stimulus condition. Viewing mounting behavior, whether male-female or female-female, increased the total number of sexual behaviors displayed, increased ejaculation frequency, and decreased latency to first mount and ejaculation, post-ejaculatory interval, and the interval between ejaculations. We conclude that male goats are aroused by the visual cues of mounting behavior, and that female-female mounting is proceptivity in goats.     

Managing the socialization of an adult male gorilla (Gorilla gorilla gorilla) with a history of social deprivation

Most non‐human primates exhibit aggression during changes in social group composition. In zoological parks, group membership changes are necessary for optimal population management, but can elicit problematic aggression. Furthermore, some primates with a long history of social deprivation are hyperaggressive when introduced to conspecifics. In this study of one male gorilla with a 30‐year history of social deprivation, we assessed the rate of aggression quantitatively during a four‐step socialization procedure. We hypothesized that 1) the frequency of agonistic/display behaviors would increase markedly at the beginning of each phase of the socialization, then decline to baseline levels over time in each phase and 2) the frequency of affiliative behaviors would not vary systematically within or between phases of socialization. Our results largely supported these predictions, and we found the four‐step socialization process effective in managing aggression in this case. In addition to documenting the successful socialization of a socially deprived adult male gorilla, we believe that the empirical process used in this case argues for scientific management of other introductions. Zoo Biol 20:347–358, 2001. © 2001 Wiley‐Liss, Inc.