Sound pressure enhances the hearing sensitivity of Chaetodon butterflyfishes on noisy coral reefs

Abstract

Butterflyfishes are conspicuous members of coral reefs that communicate with acoustic signals during social interactions with mates and other conspecifics. Members of the genus Chaetodon have a laterophysic connection (LC) -a unique association of anterior swim bladder horns and the cranial lateral line -but the action of the LC system on auditory sensitivity is unexplored. Here, we show in baseline auditory evoked potential threshold experiments that Forcipiger flavissimus (which lacks swim bladder horns and LC) is sensitive to sound tones from 100 Hz up to 1000 Hz, and that thresholds for three species of Chaetodon are 10-15 dB lower, with extended hearing ranges up to 1700-2000 Hz. The relatively high thresholds to sound pressure and low pass response near 500 Hz for all four species are consistent with a primary sensitivity to hydrodynamic particle acceleration rather than sound pressure. Deflation of the swim bladder in F. flavissimus had no measurable effect on auditory sensitivity. In contrast, displacement of gas from the swim bladder horns in Chaetodon multicinctus and Chaetodon auriga increased thresholds (decreased sensitivity) by 5-20 dB, with the greatest effect at 600 Hz. The evolution of swim bladder horns associated with the LC system in Chaetodon species has increased hearing sensitivity through sound pressure transduction in the frequency bands used for social acoustic communication. The close affiliative behaviors that are common in Chaetodon species and other butterflyfish facilitate sound perception and acoustic communication at close distances relative to the high background noise levels found in their natural reef environment.

Auditory evoked potential audiograms in post-settlement stage individuals of coral reef fishes

“…5). Previous studies have already measured behavioral audiograms in holocentrids (Tavolga and Wodinsky, 1963;Coombs and Popper, 1979), as well as AEP audiograms in a few pomacentrids (Egner and Mann, 2005;Wright et al, 2005;Wysocki et al, 2009) and chaetodontids (Webb et al, 2012;Tricas and Boyle, 2015). However, direct comparison of these studies with our AEP traces can be irrelevant because audiograms produce very different results depending on the methodology used (i.e.…”

“…During each trial, 14 different frequencies were presented: 150, 300, 600, 900, 1200, 1500, 1800, 2100, 2400, 2700, 3000, 3300, 3600 and 3900 Hz; these frequencies covered the expected range of hearing of the studied species (e.g. Coombs and Popper, 1979;Egner and Mann, 2005;Tricas and Boyle, 2015). Sound levels at each frequency were presented at up to 162 dB rms re 1 μPa and were attenuated in 6 dB steps until a threshold level was determined.…”

“…The swim bladder horns might be brought closer to the otic capsule with increasing size. For example, displacement of gas from the swim bladder horns in two Chaetodon species is known to decrease hearing sensitivity (Tricas and Boyle, 2015).…”

“…Furthermore, changes in hearing abilities may be related to the development of morphological adaptations. Some of the best-known examples were found in holocentrids and chaetodontids, in which rostral extensions of the swim bladder towards the otic capsule resulted in enhanced hearing (Coombs and Popper, 1979;Tricas and Boyle, 2015).…”

Seasonal plasticity of auditory saccular sensitivity in “sneaker” type II male plainfin midshipman fish, Porichthys notatus

“…In contrast, the pressure-mediated mode of fish hearing requires the use of specialized morphological adaptations that enable fish to transduce the pressure-induced vibrations of the swim bladder to the otolithic end organs to detect sound pressure. Otophysan fish, such as the goldfish (Carassius auratus) and zebrafish (Danio rerio), possess skeletal adaptations known as Weberian ossicles that link the swim bladder to the inner ear for enhanced pressure detection while other fishes such the Hawaiian squirrelfish (Myripristis kuntee) and the West African ladyfish (Elops lacerta) have no specialized connections between the swim bladder and inner ear, but do exhibit increased pressure sensitivity simply due to the close proximity of these gas-filled structures to the inner ear (Greenwood 1970;Coombs and Popper 1979;Braun and Grande 2008;Tricas and Boyle 2015). Additional studies have shown that natural or artificial gasfilled bladders without direct apposition to the inner ear can also significantly enhance hearing sensitivity in fishes (Chapman and Sand 1974;Jerko et al 1989).…”