Stereotypic behaviour predicts reproductive performance and litter sex ratio in giant pandas

Meghan S Martin,Guiquan Zhang,Ronald R Swaisgood,Hemin Zhang,Nathan J P Wintle,Megan Owen

doi:10.1038/s41598-020-63763-5

Abstract

Breeding and welfare problems confront many conservation breeding programs. Stereotypies—repetitive, unvarying, functionless behaviours —are common abnormal behaviours that often arise in suboptimal conditions. While the role of stereotypies in welfare assessment is well studied, few investigations address the relationship between stereotypic behaviour and reproduction. We examined the correlation between stereotypic behaviour and reproductive performance in 101 giant pandas (Ailuropoda melanoleuca). High stereotyping males copulated more and produced more cubs, suggesting that highly sexually motivated males were prone to stereotypy but also had high reproductive competence. Female stereotypies were negatively associated with all reproductive measures closely tied to behavioural competence: high stereotyping females were less likely to copulate, less likely to mother-rear cubs, and—probably a result of poor maternal care—had lower cub survival. However, females that exhibited stereotypies were more likely to produce a cub, suggesting stereotypies are tied to behavioural but not physiological competence. High stereotyping female pandas also displayed strong and consistent bias toward production of female offspring while paternal relationship to sex allocation was the reverse. These results are consistent with stress-mediated sex allocation theory. Our findings raise concern about differential reproductive success among high and low stereotyping pandas, and possible genetic adaptation to captivity.

Highlights

Breeding and welfare problems confront many conservation breeding programs
Stereotypies may be positively associated with reproductive performance because stereotypic animals: 1) are more active, resulting in better physical fitness associated with higher fertility and/or fewer birthing problems[28]; (2) have found a coping response that reduces stress, boosting hypothalamic–pituitary–gonadal axis (HPG axis) function, and reproductive output[31]; or (3) are less prone to respond to the captive environment with a depression-like state[32,33].The latter hypothesis is supported by evidence from several species indicating that individuals can respond to the environmentally induced stress either by performing frequent stereotypies or by becoming more inactive and unresponsive[31,32,33]
We examined the relationships between performance of stereotypic behaviour and several measures of reproductive performance

Summary

Introduction

Breeding and welfare problems confront many conservation breeding programs. Stereotypies— repetitive, unvarying, functionless behaviours —are common abnormal behaviours that often arise in suboptimal conditions. Animals in captivity often thrive and many species are known to survive and reproduce at rates exceeding their wild counterparts; on the other hand, many species fail to adapt to captivity and exhibit behavioural problems, reduced welfare, and poor reproduction and survival[1,2] It is perhaps unsurprising, that breeding problems are common in many captive species in zoo and conservation breeding centres: reproductive behaviour and physiology may be compromised and/or infant mortality is high[3,4,5,6,7]. By contrast stereotypic animals may have less successful reproduction because (1) highly stereotypic animals have higher stress levels which are associated with suppressed HPG axis function[34]; or (2) highly stereotypic animals are more perseverative/behaviourally disinhibited, which compromises courtship and/or maternal care[35] It is unclear which of these hypotheses may best explain the relationship between stereotypies and reproductive output, or even if they are mutually exclusive. In a zoo conservation breeding setting, we are not aware of any test of this hypothesis even though the potential impact on the demographics and sustainability of a given population is large

Methods

Results

Conclusion