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Echolocation at high intensity imposes metabolic costs on flying bats

Abstract

Vocalizations are of pivotal importance for many animals, yet sound propagation in air is severely limited. To expand their vocalization range, animals can produce high-intensity sounds, which can come at high energetic costs. High-intensity echolocation is thought to have evolved in bats because the costs of calling are reported to be negligible during flight. By comparing the metabolic rates of flying bats calling at varying intensities, we show that this is true only for low call intensities. Our results demonstrate that above 130 dB sound pressure level (SPL, at a reference distance of 10 cm), the costs of sound production become exorbitantly expensive for small bats, placing a limitation on the intensity at which they can call.

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Fig. 1: Echolocation call intensity and metabolic rate increased for nine P. nathusii flying under loud background noise (109 dB SPL) versus control conditions (69 dB SPL).
Fig. 2: The costs of increasing detection range increase rapidly above ~110 dB r.m.s. SPL (linear model fit F(1,16) = 107.06, P < 0.001).

Data availability

The datasets generated during and/or analysed during the current study are available in figshare with the identifier https://doi.org/10.6084/m9.figshare.12417113.

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Acknowledgements

Funding for this project was supported by an Alexander von Humboldt postdoctoral fellowship (S.E.C.) and the German National Research Council (Deutsche Forschungsgemeinschaft Vo890/22- CCV). We sincerely thank B. Wörle, N. Rattenborg, N. Ballerstädt, H. Goerlitz and the Max Planck Institute for Ornithology for facilitating and supporting our experiments there. We also thank L. Bailey, L. Kidd, E. Amichai and O. Mazar for constructive comments on the manuscript.

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Contributions

A.B., S.T., C.C.V. and Y.Y. designed the study. S.T. and A.B. collected the data. S.E.C. and A.B. compiled the data, conducted the analyses and wrote the first draft. C.C.V. performed blind analyses of energetics data. C.C.V. and Y.Y. contributed substantially to the writing and advised on the analyses. All authors commented on the draft.

Corresponding author

Correspondence to Shannon E. Currie.

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The authors declare no competing interests.

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Extended data

Extended Data Fig. 1 Sound spectrum.

Spectrum of sound produced under control (grey) and high background noise conditions (black).

Extended Data Fig. 2 Echolocation characteristics and metabolic rate under control and high background noise conditions.

Each bat increased a) echolocation intensity and b) metabolic rate when flying in background noise. The individual increase in metabolic rate averaged 0.05 ± 0.009 ml CO2 g-1 min-1 (range 0.01–0.09 ml CO2 g-1 min-1). c) Pulse durations also increased significantly when bats called louder in high background noise (t = −5.991, df = 8, p < 0.001). Boxes show the median (horizontal line) and interquartile range, whiskers extend to the range of the data. Colours represent individuals, grey lines connect data for individuals.

Extended Data Fig. 3 Modelled detection range of echolocation calls of Pipistrellus nathusii.

Theoretical detection range of Pipistrellus nathusii calling at 39 kHz modelled for large targets (0 dB target strength; purple solid line) and an insect target (−50 dB target strength; green dashed line). When calling above 120 dB, the increase in detection range becomes 33 cm per dB for distant targets and 15 cm per dB for an insect target (determined from the local derivatives at 130 dB).

Extended Data Fig. 4 Relationship between measured metabolic rate (CO2 production) and sodium bicarbonate measurements in resting bats.

There was a strong linear relationship between the elimination rate (kc) from sodium bicarbonate measurements and corresponding metabolic rate measured as CO2 production (VCO2) in resting bats prior to flight (VCO2 = 4.61× kc + 0.12; R2 = 0.83, p < 0.001).

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Supplementary Video 1

High-speed video of P. nathusii flying in a wind tunnel at 6 m s–1 and echolocating at one pulse per wingbeat.

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Currie, S.E., Boonman, A., Troxell, S. et al. Echolocation at high intensity imposes metabolic costs on flying bats. Nat Ecol Evol 4, 1174–1177 (2020). https://doi.org/10.1038/s41559-020-1249-8

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