Why wild giant pandas frequently roll in horse manure
- aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;
- bKey Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences/Key Laboratory of Bioactive Peptides of Yunnan Province, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223 Kunming, China;
- cCollege of Wildlife and Protected Area, Northeast Forestry University, 150040 Harbin, China;
- dCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650223 Kunming, China;
- eUniversity of Chinese Academy of Sciences, 100049 Beijing, China;
- fBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, 100044 Beijing, China
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Edited by Haoxing Xu, University of Michigan, Ann Arbor, MI, and accepted by Editorial Board Member Alan Hastings October 2, 2020 (received for review March 11, 2020)

Significance
In nature, it is extremely rare to observe attraction to fecal matter between wild mammalian species. Horse manure rolling (HMR) behavior described in this study is frequently observed in QIN pandas at low habitat temperature. Based on integrated analysis from climatic data, animal behaviors, and molecular assays, HMR is found as a temperature-, chemical-, and TRPM8-related behavior that may contribute to pandas’ cold tolerance. This study sheds light on how wild animals actively seek and utilize potential chemical resources from their habitat for survival adaptation.
Abstract
Attraction to feces in wild mammalian species is extremely rare. Here we introduce the horse manure rolling (HMR) behavior of wild giant pandas (Ailuropoda melanoleuca). Pandas not only frequently sniffed and wallowed in fresh horse manure, but also actively rubbed the fecal matter all over their bodies. The frequency of HMR events was highly correlated with an ambient temperature lower than 15 °C. BCP/BCPO (beta-caryophyllene/caryophyllene oxide) in fresh horse manure was found to drive HMR behavior and attenuated the cold sensitivity of mice by directly targeting and inhibiting transient receptor potential melastatin 8 (TRPM8), an archetypical cold-activated ion channel of mammals. Therefore, horse manure containing BCP/BCPO likely bestows the wild giant pandas with cold tolerance at low ambient temperatures. Together, our study described an unusual behavior, identified BCP/BCPO as chemical inhibitors of TRPM8 ion channel, and provided a plausible chemistry-auxiliary mechanism, in which animals might actively seek and utilize potential chemical resources from their habitat for temperature acclimatization.
Footnotes
↵1W.Z., S.Y., B.L., and Y.N. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: rlai{at}mail.kiz.ac.cn or weifw{at}ioz.ac.cn.
Author contributions: W.Z., S.Y., B.L., Y.N., R.L., and F.W. designed research; W.Z., S.Y., B.L., Y.N., A.L., X.L., R.L., and F.W. performed research; B.L., Y.N., A.L., G.H., X.L., R.L., and F.W. contributed new reagents/analytic tools; W.Z., S.Y., A.L., G.H., and F.W. analyzed data; and W.Z., S.Y., B.L., Y.N., G.H., R.L., and F.W. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission. H.X. is a guest editor invited by the Editorial Board.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2004640117/-/DCSupplemental.
Data Availability.
All data needed to evaluate the conclusions are present in this paper and/or the supporting information. Additional data are available from the authors upon request. A detailed version of this study’s materials and methods for the volatiles analysis, mimicked dunghill, transient transfection, gene synthesis, mutation, molecular modeling, and animal experiments is provided in SI Appendix. These assays were all performed using standard approaches.
Published under the PNAS license.
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