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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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.
Podos, J. & Cohn-Haft, M. Extremely loud mating songs at close range in white bellbirds. Curr. Biol. 29, R1068–R1069 (2019).
Van Belle, S., Estrada, A. & Garber, P. A. The function of loud calls in black howler monkeys (Alouatta pigra): food, mate, or infant defense? Am. J. Primatol. 76, 1196–1206 (2014).
Shen, J.-X. & Xu, Z.-M. The Lombard effect in male ultrasonic frogs: regulating antiphonal signal frequency and amplitude in noise. Sci. Rep. 6, 27103 (2016).
Surlykke, A. & Kalko, E. K. V. Echolocating bats cry out loud to detect their prey. PLoS ONE 3, e2036 (2008).
Holderied, M. W. & von Helversen, O. Echolocation range and wingbeat period match in aerial-hawking bats. Proc. R. Soc. Lond. B 270, 2293–2299 (2003).
Jakobsen, L., Brinkløv, S. & Surlykke, A. Intensity and directionality of bat echolocation signals. Front. Physiol. 4, 89 (2013).
Voigt, C. C. & Lewanzik, D. ‘No cost of echolocation for flying bats’ revisited. J. Comp. Physiol. B 182, 831–840 (2012).
Speakman, J. R. & Racey, P. A. No cost of echolocation for bats in flight. Nature 350, 421–423 (1991).
Speakman, J. R., Anderson, M. E. & Racey, P. A. The energy cost of echolocation in pipistrelle bats (Pipistrellus pipistrellus). J. Comp. Physiol. A 165, 679–685 (1989).
Winter, Y. & von Helversen, O. The energy cost of flight: do small bats fly more cheaply than birds? J. Comp. Physiol. B 168, 105–111 (1998).
Suthers, R. A., Thomas, S. P. & Suthers, B. J. Respiration, wing-beat and ultrasonic pulse emission in an echolocating bat. J. Exp. Biol. 56, 37–48 (1972).
Lancaster, W. C., Henson, O. W. & Keating, A. W. Respiratory muscle activity in relation to vocalization in flying bats. J. Exp. Biol. 198, 175–191 (1995).
Wong, J. & Waters, D. The synchronisation of signal emission with wingbeat during the approach phase in soprano pipistrelles (Pipistrellus pygmaeus). J. Exp. Biol. 204, 575–583 (2001).
Luo, J., Goerlitz, H. R., Brumm, H. & Wiegrebe, L. Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise. Sci. Rep. 5, 18556 (2015).
Hage, S. R., Jiang, T., Berquist, S. W., Feng, J. & Metzner, W. Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proc. Natl Acad. Sci. USA 110, 4063–4068 (2013).
Amichai, E., Blumrosen, G. & Yovel, Y. Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats. Proc. R. Soc. Lond. B 282, 2064 (2015).
Voigt-Heucke, S. L., Zimmer, S. & Kipper, S. Does interspecific eavesdropping promote aerial aggregations in European Pipistrelle bats during autumn? Ethology 122, 745–757 (2016).
Speakman, J. R. & Thomson, S. C. Validation of the labelled bicarbonate technique for measurement of short-term energy expenditure in the mouse. Z. Ernahrungswiss. 36, 273–277 (1997).
Troxell, S.A., Holderied, M.W., Pētersons, G. & Voigt, C.C. Nathusius’ bats optimize long-distance migration by flying at maximum range speed. J. Exp. Biol. 222, 176396 (2019).
Lancaster, W. C. & Speakman, J. R. Variations in respiratory muscle activity during echolocation when stationary in three species of bat (Microchiroptera: Vespertilionidae). J. Exp. Biol. 204, 4185–4197 (2001).
Fattu, J. M. & Suthers, R. A. Subglottic pressure and the control of phonation by the echolocating bat. Eptesicus. J. Comp. Physiol. 143, 465–475 (1981).
Šuba, J., Petersons, G. & Rydell, J. Fly-and-forage strategy in the bat Pipistrellus nathusii during autumn migration. Acta Chiropterol. 14, 377 (2012).
Kurta, A., Bell, G. P., Nagy, K. A. & Kunz, T. H. Energetics of pregnancy and lactation in freeranging little brown bats (Myotis lucifugus). Physiol. Zool. 62, 804–818 (1989).
Koblitz, J. C., Stilz, P. & Schnitzler, H.-U. Source levels of echolocation signals vary in correlation with wingbeat cycle in landing big brown bats (Eptesicus fuscus). J. Exp. Biol. 213, 3263–3268 (2010).
Kalko, E. K. V. & Schnitzler, H. U. Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behav. Ecol. Sociobiol. 33, 415–428 (1993).
Passmore, N. I. Sound levels of mating calls of some African frogs. Herpetologica 37, 166–171 (1981).
Sanvito, S. & Galimberti, F. Source level of male vocalisations in the genus Mirounga: repeatability and correlates. Bioacoustics 14, 47–59 (2003).
Nemeth, E. Measuring the sound pressure level of the song of the screaming piha Lipaugus vociferans: one of the loudest birds in the world? Bioacoustics 14, 225–228 (2004).
Wyman, M. T., Mooring, M. S., McCowan, B., Penedo, M. C. T. & Hart, L. A. Amplitude of bison bellows reflects male quality, physical condition and motivation. Anim. Behav. 76, 1625–1639 (2008).
Fletcher, N. H. A simple frequency-scaling rule for animal communication. J. Acoust. Soc. Am. 115, 2334–2338 (2004).
Fletcher, N. in Springer Handbook of Acoustics (ed. Rossing, T. D.) 785–804 (Springer, 2007).
Engel, S., Biebach, H. & Visser, G. H. Metabolic costs of avian flight in relation to flight velocity: a study in rose coloured starlings (Sturnus roseus, Linnaeus). J. Comp. Physiol. B 176, 415 (2006).
Hambly, C., Harper, E. & Speakman, J. Cost of flight in the zebra finch (Taenopygia guttata): a novel approach based on elimination of 13C labelled bicarbonate. J. Comp. Physiol. B 172, 529–539 (2002).
Hambly, C. & Voigt, C. C. Measuring energy expenditure in birds using bolus injections of 13C-labelled Na-bicarbonate. Comp. Biochem Physiol. A158, 323–328 (2011).
Butler, P. J., Green, J. A., Boyd, I. L. & Speakman, J. R. Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct. Ecol. 18, 168–183 (2004).
Pennycuick, C. J. in Avian Biology Vol. 5 (eds Farner D. S., King J. R. & Parkes K. C.) 1–75 (Academic Press, 1975).
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.
The authors declare no competing interests.
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Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
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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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