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Audible, but not ultrasonic, calls reflect surface-dwelling or subterranean specialization in pup and adult Brandt’s and mandarin voles

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Abstract

For human-audible vocalizations (below 20 kHz) of rodents, subterranean lifestyle results in low-frequency calls coupled with low-frequency hearing. For ultrasonic vocalizations (above 20 kHz), the effect of subterranean lifestyle on the acoustics is unknown. This study fills this gap of knowledge, by comparing vocalizations of two closely related species, the surface-dwelling Brandt’s vole Lasiopodomys brandtii (17 pups, 19 adults) and the subterranean mandarin vole L. mandarinus (15 pups, 16 adults). As predicted, the audible calls (AUDs) were substantially higher-frequency in L. brandtii than in L. mandarinus, in either pups or adults. In contrast to AUDs, the ultrasonic calls (USVs) did not differ in frequency variables between species, in either pups or adults. Interspecies differences were found in duration: AUDs were shorter in adult L. brandtii than in adult L. mandarinus, USVs were longer in pup L. brandtii than in pup L. mandarinus, and the low-frequency USVs of adult L. brandtii were longer than low-frequency USVs of adult L. mandarinus. We advance a hypothesis that shift towards higher-frequency AUDs in L. brandtii compared to L. mandarinus was triggered by the evolutionary emergence of the high-frequency audible alarm call, which is only present in L. brandtii but absent in L. mandarinus. We discuss that USVs may be resistant to these selection pressures as close-distant social signals.

Significance statement

Relationship between ecological specialization, such as subterranean or surface-dwelling lifestyle, and the acoustic traits of communicative signals in rodents evoke interest for over than 30 years. So far, the relationship between vocalization and subterranean life (low-frequency calls and low-frequency hearing) was only reported for calls produced by rodents in human-audible range of frequencies. No data was available for ecological adaptations of ultrasonic calls; moreover, even the existence of ultrasonic calls in subterranean rodents was unknown to recent time. Comparative studies of closely related subterranean and surface-dwelling rodent species might highlight the evolution of acoustic traits related to these ecological specializations.

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The datasets used in this study are available from the supplementary information files.

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Acknowledgements

We thank the staff of the Biological Institute of Saint Petersburg University for help and support. We thank two anonymous reviewers for their valuable and constructive comments.

Funding

This study was supported by the Russian Science Foundation grant number 19–14-00037, for the audio recording and analysis (to IAV and EVV) and by the Russian Foundation for Basic Research, grant number 19–04-00538a, for behavioral experiments with animals (to AVS).

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Authors

Contributions

IAV, AVS, and EVV designed the study. MMD, IAV, AVS, and EVV collected the data. MMD and IAV performed acoustic analyses. NAV and IAV performed statistical analyses. All authors wrote the first draft of the manuscript, commented on and approved the final manuscript before submission.

Corresponding author

Correspondence to Ilya A. Volodin.

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Ethics approval

The authors adhered to the “Guidelines for the treatment of animals in behavioural research and teaching” (Anim Behav (2020) 159:I-XI) and the legal requirements of Russia pertaining to the protection of animal welfare. The experimental procedure was approved by the Committee of Bio-ethics of Lomonosov Moscow State University, research protocol # 2011–36.

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All authors approved the final manuscript before submission.

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The authors declare no competing interests.

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Communicated by E. Korpimäki

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Dymskaya, M.M., Volodin, I.A., Smorkatcheva, A.V. et al. Audible, but not ultrasonic, calls reflect surface-dwelling or subterranean specialization in pup and adult Brandt’s and mandarin voles. Behav Ecol Sociobiol 76, 106 (2022). https://doi.org/10.1007/s00265-022-03213-6

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  • DOI: https://doi.org/10.1007/s00265-022-03213-6

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