Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (<i>gorilla gorilla</i>)

Atsalis, Sylvia; Margulis, Susan W.; Bellem, Astrid; Wielebnowski, Nadja

doi:10.1002/ajp.20010

Cited by 34 publications

(35 citation statements)

References 27 publications

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“…Demographic information from the captive gorilla population points to a combination of longevity and reduced fecundity in females as they age (Wharton and Thompson, 2000). These observations and those from our pilot study, in which longer and more variable cycle lengths occurred in older individuals, led us to suggest that gorillas may experience a perimenopause (Atsalis et al, 2004). In humans, the perimenopause is associated with decreased progesterone secretion and shorter follicular phases (Santoro et al, 1996;Weiss, 2001).…”

Section: Introductionmentioning

confidence: 91%

“…We began with a pilot study at Brookfield Zoo, in which we compared hormonal cycles, as measured via fecal progestogens, of a >40-yr-old female to sexual behaviors exhibited monthly toward the silverback male (Atsalis et al, 2004). The aged female had regular progestogen peaks that followed proceptive behavior, but her cycles were longer than those of a younger control female.…”

Section: Introductionmentioning

confidence: 99%

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Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

Atsalis

Margulis

2006

Int J Primatol

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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 1664 Atsalis and Margulis may experience a postreproductive lifespan of >25% of their lives. Continued study of aging apes is warranted, and apes may serve as models for agerelated reproductive changes in humans.

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Section: Introductionmentioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

Atsalis

Margulis

2006

Int J Primatol

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“…Alternatively, mountain gorillas with a brief PRLS may have merely become too unhealthy to give birth just before death, even if they had not undergone permanent reproductive cessation through menopause. Further study of this issue could focus on hormonal measurements of any aging females who are not nursing an infant (Atsalis et al, 2004), and autopsies when those females die (Fisher et al, 2000).…”

Section: Reproductive Terminationmentioning

confidence: 99%

“…No significant change in the total birth rate has been found through age 30 (Gerald, 1995), and reproductive cessation has not been evaluated for this population. Empirical evidence of reproductive termination was reported for 4 of 10 captive lowland gorillas who died mostly before age 30 (Caro et al, 1995), but hormonal evidence of menopause has not been detected before age 38, and some females continue cycling well into their 40s (Atsalis and Margulis, in press;Atsalis et al, 2004).…”

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confidence: 96%

Age-related patterns of reproductive success among female mountain gorillas

Robbins

Gerald-Steklis

et al. 2006

Am. J. Phys. Anthropol.

101

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A key goal of life history theory is to explain the effects of age and parity on the reproductive success of iteroparous organisms. Age-related patterns may be influenced by changes in maternal experience or physical condition, and they may reflect maternal investment trade-offs between current versus future reproduction. This article examines the influences of age and parity upon the interbirth intervals (IBI), offspring survival, and birth rates of 66 female mountain gorillas in the Virunga Volcano region from 1967-2004. Fertility was relatively low for females below age 12; improved as they matured; and then declined as they aged further. Primiparous mothers had 50% higher offspring mortality and 20% longer IBI than second-time mothers, though only the difference with IBI was statistically significant. The length of subsequent IBI was positively correlated with birth order but not with the mother's age. Mountain gorillas showed no evidence of an extended postreproductive lifespan. Age-related patterns seem most likely to reflect changes in the physical condition of the mother, but more detailed studies are needed to quantify those physical differences, and to obtain behavioral evidence that would provide more direct measures of maternal investment and experience.

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“…Diluted faecal extracts were measured for immunoreactive androgen (fA), oestrogen (fE) and progestagen (fP) metabolites using previously described enzyme immunoassay systems from Coralie Munro's laboratory at the University of California, Davis, California, USA (Graham et al 2001; deCatanzaro et al 2003;Atsalis et al 2004; Dloniak et al 2004; Fanson et al 2010a,b). We quantified fA using the testosterone polyclonal antibody R156/7, and crossreactions of relevant steroids are given in deCatanzaro et al (2003).…”

Section: Enzyme Immunoassaysmentioning

confidence: 99%

Reproductive endocrinology of zoo-housed aardwolves

et al. 2012

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Knowledge regarding the relationship between endocrine parameters and reproductive activity can offer important insights into how social and environmental factors influence the reproductive success of mammals. Although components of both the physical and social environment affect endocrine regulation of reproduction, less is understood about the potential role of interactions between different endocrine axes on reproductive activity. We evaluated temporal patterns of reproductive and adrenocortical steroids in two male and three female aardwolves (Proteles cristata) housed in captivity at Brookfield Zoo, Chicago, USA. We found seasonal variation in faecal androgens, estrogens, and progestagens, which provide support for previous observations of the aardwolf as a seasonal breeder. However, the timing of peak endocrine activity did not correspond to observations from wild populations. Our interpretation is that this discrepancy is caused by photoperiodic regulation of reproductive activity. We found a positive relationship between faecal androgens and faecal glucocorticoid metabolites in males and a positive relationship between faecal estrogens and faecal glucocorticoid metabolites in females when housed with conspecifics but not when housed alone. We also found a positive but asymptotic relationship between faecal progestagens and faecal glucocorticoid metabolites. We argue that these observations indicate a potential effect of reproductive endocrine activity on the hypothalamic-pituitary adrenal axis, which could result in interesting physiological trade-offs in male reproductive tactics and female prepartum maternal investment because of the negative effects of long-term glucocorticoid elevation on reproductive performance. Finally, our results suggest that social and environmental factors interact in regulating many aspects of endocrine fluctuations in this mostly solitary species. Key Words aardwolf, hypothalamic-pituitary adrenal axis, seasonality, stress, reproductive timingActa Theriologica, In Press 2 IntroductionKnowledge of how social and environmental factors influence animal reproductive physiology is important for our ability to understand the regulation of reproductive success. Reproductive activity in mammals is often either seasonal or non-seasonal, with subsequent different longitudinal patterns of reproductive hormones. In non-seasonal breeders, females exhibit ovulatory cycles and males are typically reproductively active throughout the year (Brown 2006). Contrarily, in seasonally breeding species reproductive hormones are elevated but highly variable during a defined period of time in both males and females (Monfort et al. 1989;Wingfield 1990;Monfort et al. 1997;Kraaijeveld-Smit et al. 2002;Kretzschmar et al. 2004;Hesterman et al. 2005; Dloniak et al. 2006b; Fanson et al. 2010a, b). The ultimate causes for seasonal breeding strategies are linked to temporal variation in resource abundance, whereas the most important proximate regulator of reproductive activity is photoperiod (Scott 1986; Gold...

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

Cited by 34 publications

References 27 publications

Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

Age-related patterns of reproductive success among female mountain gorillas

Reproductive endocrinology of zoo-housed aardwolves

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