Deep-diving pilot whales make cheap, but powerful, echolocation clicks with 50 \xb5L of air

Ilias Foskolos,Natacha Aguilar De Soto,Peter Teglberg Madsen,Mark Johnson

doi:10.1038/s41598-019-51619-6

Ilias Foskolos, Natacha Aguilar De Soto + Show 2 more

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https://doi.org/10.1038/s41598-019-51619-6

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Abstract

Echolocating toothed whales produce powerful clicks pneumatically to detect prey in the deep sea where this long-range sensory channel makes them formidable top predators. However, air supplies for sound production compress with depth following Boyle’s law suggesting that deep-diving whales must use very small air volumes per echolocation click to facilitate continuous sensory flow in foraging dives. Here we test this hypothesis by analysing click-induced acoustic resonances in the nasal air sacs, recorded by biologging tags. Using 27000 clicks from 102 dives of 23 tagged pilot whales (Globicephala macrorhynchus), we show that click production requires only 50 µL of air/click at 500 m depth increasing gradually to 100 µL at 1000 m. With such small air volumes, the metabolic cost of sound production is on the order of 40 J per dive which is a negligible fraction of the field metabolic rate. Nonetheless, whales must make frequent pauses in echolocation to recycle air between nasal sacs. Thus, frugal use of air and periodic recycling of very limited air volumes enable pilot whales, and likely other toothed whales, to echolocate cheaply and almost continuously throughout foraging dives, providing them with a strong sensory advantage in diverse aquatic habitats.

Highlights

Echolocating toothed whales produce powerful clicks pneumatically to detect prey in the deep sea where this long-range sensory channel makes them formidable top predators
In spite of the ecological importance of echolocation for toothed whales, little is known about the energetic costs of this sensory system or the behavioural and biomechanical constraints imposed by the need for continuous pneumatic sound production in deep dives[9,10]
Significant energy must be expended to dive away from the surface against the buoyancy force of air in the lungs[11], this effort yields only a small supply of air at foraging depths of deep-diving toothed whales[9]. This compressed gas is not a useful source of oxygen to fuel aerobic dives[12] and may, if managed poorly, give rise to decompression sickness[13,14]. Toothed whales reserve their limited resource of air for pneumatic sound production by sequestering air into the thick-walled tracheal and cranial spaces and distensible nasal sacs as the lungs collapse under increasing hydrostatic pressure[15,16]

Summary

Introduction

Echolocating toothed whales produce powerful clicks pneumatically to detect prey in the deep sea where this long-range sensory channel makes them formidable top predators. Air supplies for sound production compress with depth following Boyle’s law suggesting that deep-diving whales must use very small air volumes per echolocation click to facilitate continuous sensory flow in foraging dives. Definitive evidence for recycling is absent[17], it is assumed to occur during occasional pauses in echolocation[18] If this is correct, deep-diving whales face an apparent tradeoff in how they use air for sound production: www.nature.com/scientificreports investing larger air volumes per click presumably gives greater acoustic output, and increased prey detection range, but necessitates frequent recycling and interruption of sensory flow during foraging. Animals in both studies had uncompressed lungs and abundant air available for clicking, making the results of questionable relevance to deep-diving echolocators

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