Abstract

The physiologic basis for puberty and reproductive senescence is virtually unknown in felids. For many nondomestic cat species, studbook records listing the youngest and oldest ages for reproduction represent the only information available on reproductive maturity and age-related decline but even these limited data can be confounded by management practices. In this study, we investigated the waxing and waning of reproductive function in the Pallas’ cat (Otocolobus manul), a small-sized felid native to Central Asia that exhibits pronounced reproductive seasonality restricted to the winter months. Our specific objectives were to 1) characterize pubertal changes in morphologic, hormonal, and seminal traits in juvenile male and female Pallas’ cats and 2) compare ovarian responsiveness, oocyte metabolism, and embryo development in young versus old females. For the puberty study, juvenile cats (n=four males, two females) were anesthetized bimonthly beginning in late fall for blood sampling, body measurements ± electroejaculation for semen analysis. Fecal samples were analyzed for testosterone, estrogen, and/or progesterone metabolites and serum was assessed for leptin, thyroxine (T4) and luteinizing hormone (LH). For the reproductive senescence study, female Pallas’ cats (n=4) in two age cohorts (1–4 years and >6 years) were treated during two breeding seasons with exogenous gonadotropins (300 IU eCG followed 86 hours later with 150 IU hCG) and subjected to laparoscopy to evaluate ovarian follicular responses and recover oocytes for metabolism assessment (glycolysis, pyruvate oxidation), in vitro fertilization and embryo culture.

Spermic ejaculates were recovered from all males by 7–10 months of age, corresponding to increases in fecal testosterone beginning 1–2 months earlier and concurrent with increases in body mass and leptin levels. T4 (range, 17–37 nmol/L) and LH (range, 1.99–3.80 ng/ml) concentrations were variable throughout puberty. Male body mass peaked from December to February before declining rapidly by May. Both females displayed estrous cyclicity and mating behavior by 10–11 months of age, with both showing increases in fecal progesterone indicative of ovulation. One female became pregnant and gave birth to six viable kittens after a ∼68-day gestation. Comparing young to old cats, there were no differences (p>0.05) in mean (+ SEM) number of ovarian follicles (16.3+3.3 vs. 12.8+2.9) or % of good-quality oocytes (89.2% vs. 87.8%), and high (67–90%) fertilization percentages were obtained in both cohorts. Oocyte glucose metabolism was similar (p>0.05) between age groups but pyruvate oxidation was increased (p<0.001) in oocytes from older (1.46 pmol/oocyte/3 h) vs. younger (0.52 pmol/oocyte/3 h) females. Fewer (p<0.05) IVF embryos from older (29%, 5/17) than younger (80%, 16/20) cats developed to morulae during culture. These results indicate that both male and female Pallas’ cats can become reproductively mature by 10 months of age with mating and offspring production during their first breeding season following birth. Findings also suggest that alterations in oocyte metabolism and embryo development may be responsible for decreased fecundity after 6 years of age. These findings may have important implications for reproductive management of captive Pallas’ cat populations as well as improving our understanding of the ecology of Pallas’ cats in the wild.

Acknowledgments

The assistance of the veterinary and animal care staff at the Cincinnati Zoo & Botanical Garden and North Carolina State University is gratefully acknowledged. This study was funded, in part, by a grant (D04ZO-30) from the Morris Animal Foundation.