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Research Article

Why wild giant pandas frequently roll in horse manure

View ORCID ProfileWenliang Zhou, View ORCID ProfileShilong Yang, View ORCID ProfileBowen Li, View ORCID ProfileYonggang Nie, Anna Luo, Guangping Huang, Xuefeng Liu, View ORCID ProfileRen Lai, and View ORCID ProfileFuwen Wei
  1. aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;
  2. 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;
  3. cCollege of Wildlife and Protected Area, Northeast Forestry University, 150040 Harbin, China;
  4. dCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650223 Kunming, China;
  5. eUniversity of Chinese Academy of Sciences, 100049 Beijing, China;
  6. fBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, 100044 Beijing, China

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PNAS December 22, 2020 117 (51) 32493-32498; first published December 7, 2020; https://doi.org/10.1073/pnas.2004640117
Wenliang Zhou
aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;
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  • ORCID record for Wenliang Zhou
Shilong Yang
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;
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Bowen Li
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;
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  • ORCID record for Bowen Li
Yonggang Nie
aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;
dCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 650223 Kunming, China;
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Anna Luo
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;
eUniversity of Chinese Academy of Sciences, 100049 Beijing, China;
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Guangping Huang
aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;
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Xuefeng Liu
fBeijing Key Laboratory of Captive Wildlife Technologies, Beijing Zoo, 100044 Beijing, China
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Ren Lai
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;
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  • For correspondence: rlai@mail.kiz.ac.cn weifw@ioz.ac.cn
Fuwen Wei
aKey Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, 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;
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  • For correspondence: rlai@mail.kiz.ac.cn weifw@ioz.ac.cn
  1. 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)

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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.

  • giant panda
  • horse
  • feces
  • TRPM8
  • temperature

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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Why wild giant pandas frequently roll in horse manure
Wenliang Zhou, Shilong Yang, Bowen Li, Yonggang Nie, Anna Luo, Guangping Huang, Xuefeng Liu, Ren Lai, Fuwen Wei
Proceedings of the National Academy of Sciences Dec 2020, 117 (51) 32493-32498; DOI: 10.1073/pnas.2004640117

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Why wild giant pandas frequently roll in horse manure
Wenliang Zhou, Shilong Yang, Bowen Li, Yonggang Nie, Anna Luo, Guangping Huang, Xuefeng Liu, Ren Lai, Fuwen Wei
Proceedings of the National Academy of Sciences Dec 2020, 117 (51) 32493-32498; DOI: 10.1073/pnas.2004640117
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