“Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion,” by S. Atsalis and E. Videan, American Journal of Primatology 71, 271–282 (2009)

Abstract

Atsalis and Videan [2009] conclude that the ‘‘occurrence of a postreproductive life span [is] more evident in some species of captive populations that can live for a long time beyond what is foreseen by the follicular store.’’ Specifically, they contend that captivity causes chimpanzees to undergo more ovulations than do chimpanzees in the wild, so that they experience menopause earlier. Central to this contention is the premise that ‘‘despite the increased longevity generally observed in captive populations reproductive life span is shortened.’’ We point out in this commentary that most published evidence on the timing of menopause in chimpanzees, including our own work, contradicts this premise, instead suggesting that menopause occurs late in the life span of the captive chimpanzee. The authors cite Emery Thompson et al. [2007] as support for their claim that chimpanzees reproduce into their 40s in the wild. The conclusion that menopause has occurred by age 40 in captive chimpanzees is based upon a study by Videan et al. [2006], which claimed that menopause occurs at 35–40 years of age in the chimpanzees. This conclusion was not based upon observation of menses or cycles of ovulation, but rather upon determination of gonadotrophin levels in two samples each year obtained from 14 female chimpanzees, 3 of which were over the age of 40. The criterion for menopause was the presence of FSH levels greater than 14 IU/ mL. The conclusion that menopause is reached between 35 and 40 years of age was based upon mean FSH in each age group. Studies using other methods have reached different conclusions. The first published study on reproductive aging in captive chimpanzees [Graham, 1979] examined ten female chimpanzees aged 35–48 years old at the Yerkes National Primate Research Center (YNPRC). At least one menstrual cycle was observed within 1 year of death in each of these individuals. In a subsequent study, also conducted at the YNPRC, Gould et al. [1981] observed two common chimpanzees and one bonobo over the age of 40. They concluded that the bonobo (Pan paniscus) was menopausal, based on cessation of menses and anogenital swelling, elevated gonadotropins and ovarian histology. Unfortunately, the precise age of this individual was unknown. Importantly, the two common chimpanzees (Pan troglodytes) continued to experience menstrual cyclicity at ages 48 and 50. Our larger study of menstrual cycles in 89 chimpanzees at the YNPRC [Lacreuse et al., 2008] confirms the findings of Gould et al. [1981] and contradicts the findings of the Videan et al. [2006]. Our study was based upon observations of cycles of menstrual bleeding and included observations of 20 individuals past the age of 40 years; all 20 of these individuals displayed menstrual cycles after the age of 40; one chimpanzee gave birth at the age of 42, two years past the age suggested as the age of menopause for captive chimpanzees. Since this birth occured in the same year (1997) that the US moratorium on chimpanzee breeding was begun, we do not know whether births may have occurred at even later maternal ages. Indeed, a recent paper reports that a chimpanzee in a zoo in Switzerland gave birth to a healthy infant at a documented age of 49 years; this chimpanzee’s only other infant (to date!) was born when the mother was 42 [Puschmann & Federer, 2008]. This late fertility is consistent with our population at YNPRC, where