Sylvia Atsalis

Behavioral monitoring in zoos and aquariums: a tool for guiding husbandry and directing research.

Behavioral monitoring is the scientific collection of animal behavior data to understand normal patterns of behavior and changes in these patterns. This tool is underutilized in the zoo industry although it can be an effective indicator of many potential problems that compromise zoo animal well-being. We suggest that a behavioral monitoring program should be a core component of a zoological institutions care program. We detail the benefits of such a program and describe its components. We provide guidelines for implementing such a program and make recommendations that will help institutions to employ behavioral monitoring programs with reasonable expense. We argue that the benefits of such a program, primarily increased detection of rising or potential problems, far outweigh the minor costs of implementation.

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009.

Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

As our closest living relatives, great apes likely experience behavioral and physiological patterns associated with reproductive aging and menopause that are similar to human patterns. We present results from a nationwide zoo-based study on behavioral and hormonal changes in female western gorillas. We evaluated progestogen concentrations via daily fecal sampling in 30 gorillas, 22 of which were geriatric (≥30). We collected concurrent behavioral data 1–3 times weekly on 16 of the females. While control females cycled regularly, ca. 23% of geriatric females are acyclic (menopausal), and another 32% show variable hormonal patterns suggesting perimenopause. Patterns included increased variability in cycle length and peak progestogen values, and frequent insufficient increases in progestogen levels during the luteal phase. Acyclic females have significantly lower overall progestogen concentrations than the self cycling females, though differences are not significant when cycle phase is incorporated. We detected behavioral estrus in 9 of 10 cycling females for which data were available. In all but 1 case, proceptive behavior occurred during the follicular phase, preceding ovulation on average by 6.6 d. Females spent more time in proximity to the silverback male while in behavioral estrus than during other periods. To date, maximum longevity in captive female gorillas is 52 yr, with poor reproductive prognosis beginning from the age of 37. We demonstrate that both perimenopause and menopause characterize aged female gorillas, which may experience a postreproductive lifespan of >25% of their lives. Continued study of aging apes is warranted, and apes may serve as models for age-related reproductive changes in humans.

Perimenopause and Menopause: Documenting Life Changes in Aging Female Gorillas

As our closest living relatives, great apes likely experience physiological patterns associated with reproductive aging that are similar to humans. We present results from a nationwide zoo-based study on female western lowland gorillas during which we evaluated concentrations of progestogens via daily fecal sampling in 30 gorillas, 22 of whom were geriatric (>or=30). Whereas control females cycled regularly, ca. 23% of geriatric females were acyclic (menopausal), and approximately 1/3 showed variable hormonal patterns suggestive of perimenopause. Patterns included increased cycle variability, low luteal phase rises of progestogens - possibly indicative of anovulatory cycling - and peak height variability of progestogens in the luteal phase of the cycle. We discovered a progressive trend toward increased variability in estrous cycle length and toward decreased concentrations of fecal progestogens when we compared control to geriatric cycling and to geriatric noncycling females. Noncycling females had significantly lower overall progestogen concentrations than the cycling females, though differences were not significant when cycle phase was incorporated. Preliminary analyses of follow-up data on 10 perimenopausal females indicated that subjects experienced age-related changes in reproductive function that mirrored those observed in aging human females including a female who transitioned from perimenopause to menopause. To date, maximum longevity in captive female gorillas is 52 years, with poor reproductive prognosis beginning from the age of 37 suggesting a postreproductive lifespan of >25%. Continued study of aging apes is warranted, with emphasis on longitudinal monitoring of aged subjects.

Primate Reproductive Aging: From Lemurs to Humans

The scope of data now available for primates from long-term field and captive studies has opened up exciting possibilities for investigating age-related patterns of reproduction. Valuable information on the aging process can be gleaned through broad cross-taxonomic comparative studies that include lemurs, monkeys, apes and humans. Thus, across all taxa discussed in this volume, female reproduction was found to be complex and dynamic, affected by the interplay of multiple exogenous and endogenous factors. Throughout their lives, females differ in their individual reproductive output. As they age, a period of reproductive instability is common among female primates and perimenopausal- like hormonal changes have been noted in many species. Available data from lemurs and callitrichids indicate that at least in some species, age-related declines in reproduction are manifested as diminished success of females to rear their young to weaning age. Few data are available for New World primates, but the same observation holds true for Old World monkey females, who also are characterized by declines in sexual activity and decreased birth rates. In apes, captive data suggest the presence of an appreciable postreproductive lifespan but this has not been confirmed in the wild. Menopause may be manifested as an evolutionary continuum across primate taxa with the potential for an extended postreproductive lifespan evident in cercopithecines and apes.

Assessment of reproductive behavior and hormonal cycles in geriatric western Lowland gorillas

The population of western lowland gorillas in North American zoos is aging and, as is the case with the aging human population, may have unique physical and social needs. We have documented previously that 25% of aging females (5/22) ceased to show reproductive cycles entirely, and could be defined as menopausal. Approximately 32% of females showed somewhat irregular cycling patterns. We review our hormonal and behavioral findings on reproductive aging in gorillas; describe the range of cycling patterns that we see and how we interpret these; and discuss the implications of these findings for captive management and husbandry of aging gorillas. We monitored fecal hormone metabolites (progestogens) in 30 gorillas and collected simultaneous behavioral data to evaluate the relationship between cyclicity and sexual behavior. We identified and described several discrete patterns of irregular cycling. These included extreme variability of cycle length, cyclic patterns with unusually low progestogen peak concentrations that possibly may not support luteal activity, and large variability in maximum progestogen peak height among cycles. All of these changes are consistent with age-related hormonal changes observed in humans and may be signs of changes in fertility as well. Behaviorally, nearly all cycling females exhibited signs of estrus. Affiliative behavior between male silverbacks and estrous females was observed in the control females, but not the geriatric females. These findings suggest that pre-menopausal females are exhibiting signs of perimenopause. As is the case in humans, such changes in hormone patterns may occur years before the onset of menopause. As enhancements in nutrition, husbandry, and veterinary medicine have led to increased longevity in our zoo populations of apes, it has become imperative that we investigate and better understand associated physiological and behavioral changes in geriatric animals to ensure appropriate management of this increasing demographic sub-population. Zoo Biol 0:1-23, 2007. (c) 2007 Wiley-Liss, Inc.

Effects of combination birth control on estrous behavior in captive western lowland gorillas, Gorilla gorilla gorilla.

Combination birth control pills (CBC) are one of the most common birth control methods used for western lowland gorillas (Gorilla gorilla gorilla) housed in zoos. Since zoos are interested in maintaining as many natural behaviors as possible, it is important to know how contraception may affect social and sexual interactions among group members. Although some data are available regarding the influence of the pill on sexual behavior in human females, no data are available on its effects on gorilla estrous behavior. We examined temporal trends of estrous, aggressive, affiliative, and activity budget data in four females on CBC at the Lincoln Park Zoo in Chicago, IL. Behavioral data were collected using point sampling, all-occurrence records, and one-zero sampling. Estrous behavior occurred in less than 1% of observations. Using all-occurrence and one-zero sampling, estrous behavior occurred more frequently in week one of the cycle than any other week. The focal females exhibited affiliative, aggressive, and activity budget data evenly across their cycles. There were also no temporal trends in proximity to the silverback. Females varied by the types of estrous behavior they exhibited. We give a hormonal explanation for the prevalence of estrous behaviors in week one, and recommendations for effective behavioral sampling of gorilla estrous behavior.