Motile Sperm Output by Male Cheetahs (Acinonyx jubatus) Managed Ex Situ Is Influenced by Public Exposure and Number of Care-Givers

Abstract

The collective cheetah (Acinonyx jubatus) population in zoological institutions has never been self-sustaining because of challenges in natural reproduction. A retrospective analysis of North American zoo-breeding records has revealed that >90% of litters produced since 2003 occurred in facilities ‘off-display’ from the public. We examined seminal, endocrine, and behavioral traits of 29 adult male cheetahs that were: 1) managed in public exhibit or off-display facilities; 2) maintained by different numbers of cheetah-specific care-givers; and 3) living adjacent to varying numbers of adult conspecifics. Cheetahs housed off-display produced more total motile sperm/ejaculate (P = 0.04) than on-exhibit males. This finding was mirrored in our laboratory’s historical records where two-fold more total motile sperm (P < 0.01) were measured in ejaculates from individuals with no public exposure (n = 43) compared to on-exhibit (n = 116) counterparts. Males at institutions with ≤3 care-givers also produced more total motile sperm/ejaculate (P < 0.03) and spent more time behaviorally active (P < 0.01) than at facilities using >3 care-givers. Exposure to high numbers of conspecifics within the same institution did not impact (P > 0.05) seminal traits, and presence of the public, care-giver number, or animals/facility had no influence (P > 0.05) on androgen or glucocorticoid excretion or other behavioral metrics. Findings indicate that male cheetahs are sensitive to general public exposure and too many care-givers, resulting in compromised motile sperm output/ejaculate with mechanism of action unrelated to altered androgen or glucocorticoid excretion.

Glucocorticoids and Reproduction: Traffic Control on the Road to Reproduction

“…Fertility in both male and female cheetahs is sensitive to the physiological stress that accompanies captivity. Living arrangements on-exhibit compared to off-exhibit increased glucocorticoid concentrations, reduced total mobile sperm numbers in males, and decreased ovarian cyclicity in females [166, 167]. Heat stress leads to infertility in dairy cows by inhibiting follicular development.…”

Group management influences reproductive function of the male cheetah (Acinonyx jubatus)

“…There is no effect of circannual seasonality on cheetah ejaculate quality (Crosier et al 2007;Koester et al 2015). For the present study, semen was collected once per male beginning at least 2 months after fecal sampling commenced for endocrine monitoring (see below).…”

“…Androgen metabolite concentrations in diluted fecal extracts were determined using a testosterone EIA previously validated for use in the cheetah (Koester et al 2015). This EIA relies on a polyclonal anti-testosterone antibody (R156/7; C. Munro, University of California, Davis, CA, USA) that cross-reacts with testosterone (100%), 5a-dihydrotestosterone (57.4%), ,1% with androstenedione, androsterone, androsteneolone, cholesterol and oestradiol-17b and ,0.02% with progesterone, pregnenolone and hydrocortisone.…”

“…Fecal glucocorticoid metabolite analysis Glucocorticoid metabolite concentrations in diluted fecal extracts were determined using a cortisol EIA validated earlier for the cheetah (Young et al 2004;Koester et al 2015). The polyclonal antibody used (R4866; C. Munro) was raised in rabbits against cortisol-3-carboxymethyloxime linked to BSA.…”

“…Genetically appropriate males and females are then introduced together in pairings for brief periods, depending on annual SSP breeding recommendations and, of course, sexual receptivity signals offered by the female; the pair is separated post-mating. Our laboratory has studied the reproductive metrics of cheetahs in nature and captivity for decades, with emphasis on physiological norms and uniqueness (Wildt et al 1983(Wildt et al , 1988Brown et al 1996;Wielebnowski and Brown 1998;Crosier et al 2007Crosier et al , 2011, the application of various assisted reproductive approaches (Howard et al , 1997Wildt and Roth 1997;Crosier et al 2006) and, more recently, factors that may be contributing to low reproductive success under ex situ conditions (Wielebnowski et al 2002b;Koester et al 2015). Recently, we have discovered that exposing cheetahs to traditional public exhibits as well as to more than three caregivers reduces sperm output (the total numbers of motile spermatozoa per ejaculate) and overall behavioural activity compared with males housed in spacious breeding centres away from people (Koester et al 2015).…”