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Geographical variation in squirrel mating calls and their recognition limits in the widely distributed species complex

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Abstract

Acoustic signals are one of the reproductive isolation mechanisms that can be a driving force for speciation. Evidence that geographic variation in mating calls can cause reproductive isolation is abundant for birds and frogs, but not for mammals. In the Callosciurus genus of tree squirrels distributed in Southeast Asia, males emit mating calls to attract females and the sound properties are known to be distinctly different among coexisting congeneric species. We investigated whether mating calls emitted by males differ between ten populations of the widely distributed C. erythraeus/C. finlaysonii complex. Based on the acoustic properties, the populations were divided into four groups (South Vietnam, Taiwan, eastern China, and western areas including Thailand and western China), which resulted in a high discrimination rate of 94.7% by a discriminant function analysis. A playback experiment was also conducted to determine whether the mating calls from different localities were as effective in attracting conspecific individuals as those in the same locality. In Kanagawa, Japan, where squirrels were introduced from Taiwan in the 1950s, squirrels responded more frequently to the playback sounds recorded in Taiwan compared to those recorded in Thailand. In addition, the response of squirrels decreased with an increase in the difference in acoustic characteristics compared to that from the original habitat. These results suggest that local differences in acoustic characteristics could be one of the mechanisms that promote reproductive isolation of geographically distant populations of Callosciurus.

Significance statement

Acoustic signals are one of the reproductive isolation mechanisms that can be a driving force for speciation. The tree squirrel genus Callosciurus (Sciuridae) is widely distributed in Southeast Asia and is one of the few suitable mammals for testing the premating isolation mechanism using acoustic signals. The mating calls of the C. erythraeus/C. finlaysonii complex were divided into four geographical groups (Taiwan, Vietnam, eastern China, and Thailand) by a discriminant function analysis. Playback experiments revealed that the squirrels responded more frequently to the sounds of their own group compared to those of other groups. In addition, the response of the squirrels decreased with an increase in the difference in acoustic characteristics compared to that from the original habitat. Local differences in acoustic characteristics could be one of the mechanisms that promote reproductive isolation of geographically distant populations of Callosciurus.

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Acknowledgments

We are grateful H.S. Yong (University of Malaya), B. Kanchanasaka (Department of National Park Wildlife and Plant Conservation), P. Pipat (Chulalongkorn University), Y. Peng (Xishuangbanna Tropical Botanical Garden), and R. Tabuchi (Forest Products Research Institute) for making our study possible and E. Ohya (Forest Products Research Institute) for providing valuable advice regarding the acoustic analyses. We also thank the assistance provided by the staff of the following station: Ulu Gombak Field Station, Khao Ang Runai Wildlife Conservation, Khao Kheow Wildlife Sanctuary, Doi Suthep National Park, and Yokohama Nature Sanctuary. This study was financially supported by the Bureau of Industrial and Labor Affairs, Tokyo Metropolitan Government, and Forestry and Forest Products Research Institute, Japan. Comments from the editor and anonymous reviewers improved an earlier version of this manuscript.

Funding

This study was financially supported by the Bureau of Industrial and Labor Affairs, Tokyo Metropolitan Government, JSPS KAKENHI Grant Number 18H02247, and Forestry and Forest Products Research Institute, Japan.

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Authors and Affiliations

  1. Tama Forest Science Garden, Forestry and Forest Products Research Institute, Todori 1833-81, Hachioji, Tokyo, 193-0843, Japan

    Noriko Tamura

  2. Department of National Park Wildlife and Plant Conservation, Bangkok, Thailand

    Phadet Boonkhaw & Umphornpimon Prayoon

  3. Center for Entomology & Parasitology Research, Duy Tan University, Da Nang, Vietnam

    Quoc Toan Phan

  4. Department of Biology, Tokyo Metropolitan University, Tokyo, Japan

    Pei Yu & Fumio Hayashi

  5. Department of Entomology, China Agricultural University, Beijing, China

    Xingyue Liu

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  1. Noriko Tamura
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Contributions

NT conceived and planned the study, conducted the experiment, collected data in the field, performed statistical analyses, interpreted results, and wrote the first draft of the manuscript; PB, UP, QTP, PY, XL, and FH collected data in the field and contributed to the interpretation of the results. All authors read and approved the final manuscript.

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Correspondence to Noriko Tamura.

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All applicable international, national, and/or institutional guidelines for conducting research were followed. According to ‘Act on Welfare and Management of Animals’ by the Ministries of Environment, Government of Japan, playback experiments at the present study site do not fall within the authority of the Local Ethical Commission in Japan and its approval was not required (www.env.go.jp/en/laws/nature/index.html). Playback trials were kept brief to minimize disturbance to our subjects. The sound power was adjusted to the level which was the same as the natural sounds.

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Tamura, N., Boonkhaw, P., Prayoon, U. et al. Geographical variation in squirrel mating calls and their recognition limits in the widely distributed species complex. Behav Ecol Sociobiol 75, 97 (2021). https://doi.org/10.1007/s00265-021-03022-3

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