Changes in urinary androgen concentration indicate that male giant pandas (Ailuropoda melanoleuca) respond to impending female oestrus during and outside the typical spring breeding season

Abstract

Giant pandas have been described as mono-oestrus spring breeders, yet males exposed to aseasonal oestrous females in the autumn or winter exhibit breeding behaviours and interest in mating. In the present study, urinary androgens and sperm parameters were quantified for males exposed to females expressing oestrus during spring, autumn or winter to examine plasticity of reproductive seasonality in giant pandas. Monthly average androgen concentrations for two males exposed to females in either seasonal or aseasonal oestrus were greater (P<0.001) than baseline concentrations. Evaluation of daily androgen concentrations revealed a peak that was three- to fivefold greater than baseline, occurring an average of 5 days before ovulation for both seasonal and aseasonal cycles. There were no significant differences in testes volume, sperm motility, forward progression or sperm concentration in males between female seasonal and aseasonal cycle years. Male gonadal activity was more variable without a clear pattern in years when the female was anovulatory than when she was ovulatory (seasonal or aseasonal). These data show the flexible reproductive capacity of male giant pandas as demonstrated by a rapid physiological readiness to mate in response to female oestrous cues within or outside the normal breeding season and may suggest a facultative seasonal reproduction with a 'female-induced rut'.

The novel use of urinary androgens to optimise detection of the fertile window in giant pandas

“…We developed and validated testosterone and DHEA assays to measure androgens in giant panda urine. Testosterone metabolites have been previously measured in male giant panda urine ( MacDonald et al 2006 , Steinman et al 2006 , Kersey et al 2010 c , Gocinski et al 2018 ); however, the biological validation step in our study provides the first measurement of male giant panda urinary androgens with a DHEA assay. In the intact male, DHEA showed a seasonal profile close to that of testosterone.…”

Immune profiles of male giant panda (Ailuropoda melanoleuca) during breeding season

“…Animals in nature need to balance resource allocation between reproduction and self-maintenance, and immunity is a major component of self-maintenance [22]. The reproduction and conservation of giant pandas has been, and continues to be, of global concerns [12,23]. Our research group's previous work investigated immune changes at four key phases of female giant panda reproduction [11].…”

Simultaneous choice bioassays accompanied by physiological changes identify civetone and decanoic acid as pheromone candidates for giant pandas

“…Giant pandas typically breed during the spring months (Schaller et al, 1985); however, males undergo physiological changes in preparation for the mating season starting in October (Aitken‐Palmer et al, 2012). Furthermore, androgen concentrations have been shown to increase in males during the fall when housed with a female undergoing fall estrus and males have demonstrated rapid physiological changes to mate during and outside the breeding season (Gocinski et al, 2018). In the current study, males may be responding to the stimuli during the fall in preparation for the mating season.…”

“…The concentration of androgen metabolites (ng androgen/mg creatinine) in male giant panda urine was determined using a single antibody competitive enzyme immunoassay at the Memphis Zoo as previously described (Gocinski et al, 2018; Knott et al, 2013; Knott, Mastromonaco, Owen, & Kouba, 2017; Wilson et al, 2018). The concentration of creatinine mg/ml in urine was used to account for variations in water content between samples.…”