Surviving winter on the Qinghai-Tibetan Plateau: Pikas suppress energy demands and exploit yak feces to survive winter

John R. Speakman*, Qingsheng Chi, Łukasz Ołdakowski, Haibo Fu, Quinn E. Fletcher, Catherine Hambly, Jacques Togo, Xinyu Liu, Stuart B. Piertney, Xinghao Wang, Liangzhi Zhang, Paula Redman, Lu Wang, Gangbin Tang, Yongguo Li, Jianguo Cui, Peter J. Thomson, Zengli Wang, Paula Glover, Olivia C. RobertsonYanming Zhang, Dehua Wang

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

32 Citations (Scopus)

Abstract

The Qinghai-Tibetan Plateau, with low precipitation, low oxygen partial pressure, and temperatures routinely dropping below −30 °C in winter, presents several physiological challenges to its fauna. Yet it is home to many endemic mammalian species, including the plateau pika (Ochotona curzoniae). How these small animals that are incapable of hibernation survive the winter is an enigma. Measurements of daily energy expenditure (DEE) using the doubly labeled water method show that pikas suppress their DEE during winter. At the same body weight, pikas in winter expend 29.7% less than in summer, despite ambient temperatures being approximately 25 °C lower. Combined with resting metabolic rates (RMRs), this gives them an exceptionally low metabolic scope in winter (DEE/RMRt = 1.60 ± 0.30; RMRt is resting metabolic rate at thermoneutrality). Using implanted body temperature loggers and filming in the wild, we show that this is achieved by reducing body temperature and physical activity. Thyroid hormone (T3 and T4) measurements indicate this metabolic suppression is probably mediated via the thyroid axis. Winter activity was lower at sites where domestic yak (Bos grunniens) densities were higher. Pikas supplement their food intake at these sites by eating yak feces, demonstrated by direct observation, identification of yak DNA in pika stomach contents, and greater convergence in the yak/pika microbiotas in winter. This interspecific coprophagy allows pikas to thrive where yak are abundant and partially explains why pika densities are higher where domestic yak, their supposed direct competitors for food, are more abundant.

Original languageEnglish
Article numbere2100707118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number30
DOIs
Publication statusPublished - 27 Jul 2021

Bibliographical note

Data Availability
The data have been deposited in the Open Science Framework (https://osf.io/vg3mc/).

Funding Information:
Key Research and Development Program of China (Grant 2016YFC0501905-04), and a United Kingdom–China collaboration grant from the Royal Society and National Science Foundation of China (NSFC-RS 30711130224). J.R.S. was also supported by the President’s International Fellowship Initiative professorial fellowship program and a Wolfson merit award. Ł.O. was supported by a PIFI2017 (Presidents International Fellowship Initiative 2017).

Keywords

  • Metabolic suppression
  • Thyroid axis
  • Winter survival

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