Potential for Sound Sensitivity in Cephalopods

Mooney, T. Aran; Hanlon, Roger T.; Madsen, Peter T.; Christensen‐Dalsgaard, Jakob; Ketten, Darlene R.; Nachtigall, Paul E.

doi:10.1007/978-1-4419-7311-5_28

Cited by 11 publications

(8 citation statements)

References 17 publications

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“…Recent research supports earlier hypotheses of sound detection by squid (Hanlon and Budelmann, 1987;Mooney et al, 2010Mooney et al, , 2012Kaifu et al, 2011). Sound detection is thought to be mediated by the squid statocyst, an evolutionarily ancient sensory system that is primarily a gravity detector and accelerometer (Budelmann, 1990).…”

Section: Introductionsupporting

confidence: 74%

“…In vertebrates, aminoglycosides are thought to enter auditory hair cells through the mechanotransduction channel at the tips of the stereociliary bundles and increase reactive oxygen species within the cell, ultimately leading to apoptosis (Huth et al, 2011). The squid statocyst is primarily a vestibular sensory system, but it also may function as a primitive auditory system (Budelmann, 1979(Budelmann, , 1990Mooney et al, 2010Mooney et al, , 2012. Due to the combined vestibular/auditory nature of the statocyst and the heterogeneity of hair cell types in the statocyst, aminoglycoside damage may differ across the epithelium.…”

Section: Discussionmentioning

confidence: 99%

“…The statocyst is analogous to the fish otolith system (Fay, 1974) and, to some extent, may share functions of the inner ear hair cells of higher vertebrates (Yost, 1994). Because squid are now considered to respond to some acoustic components, there is concern that increases in ocean noise may damage statocyst hair cells and impact their hearing (Packard et al, 1990;Budelmann et al, 1992;Kaifu et al, 2008;Hu et al, 2009;André et al, 2011;Mooney et al, 2012;Solé et al, 2013). Additionally, squid have been a model species in physiology and neuroscience since the classic experiments by Hodgkin and Huxley on the nature of the action potential Huxley, 1945, 1952), and their use is growing in other areas such as the study of camouflage and animal-bacterial symbioses (Hanlon, 2007;Lee et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Aminoglycoside-Induced Damage in the Statocyst of the Longfin Inshore Squid, Doryteuthis pealeii

Scharr

Mooney

Schweizer

et al. 2014

The Biological Bulletin

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Abstract. Squid are a significant component of the marine biomass and are a long-established model organism in experimental neurophysiology. The squid statocyst senses linear and angular acceleration and is the best candidate for mediating squid auditory responses, but its physiology and morphology are rarely studied. The statocyst contains mechano-sensitive hair cells that resemble hair cells in the vestibular and auditory systems of other animals. We examined whether squid statocyst hair cells are sensitive to aminoglycosides, a group of antibiotics that are ototoxic in fish, birds, and mammals. To assess aminoglycoside-induced damage, we used immunofluorescent methods to image the major cell types in the statocyst of longfin squid (Doryteuthis pealeii). Statocysts of live, anesthetized squid were injected with either a buffered saline solution or neomycin at concentrations ranging from 0.05 to 3.0 mmol l Ϫ1 . The statocyst hair cells of the macula statica princeps were examined 5 h post-treatment. Anti-acetylated tubulin staining showed no morphological differences between the hair cells of saline-injected and non-injected statocysts. The hair cell bundles of the macula statica princeps in aminoglycoside-injected statocysts were either missing or damaged, with the amount of damage being dose-dependent. The proportion of missing hair cells did not increase at the same rate as damaged cells, suggesting that neomycin treatment affects hair cells in a nonlethal manner. These experiments provide a reliable method for imaging squid hair cells. Further, aminoglycosides can be used to induce hair cell damage in a primary sensory area of the statocyst of squid. Such results support further studies on loss of hearing and balance in squid.

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Section: Introductionsupporting

confidence: 74%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Aminoglycoside-Induced Damage in the Statocyst of the Longfin Inshore Squid, Doryteuthis pealeii

Scharr

Mooney

Schweizer

et al. 2014

The Biological Bulletin

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“…The differences between the physiology and behavior results could reflect that the evoked potential methods are not as sensitive as the animal's auditory system and these behavioral metrics. Or there could be taxonomybased differences as this study used cuttlefish, while Kaifu et al (Kaifu et al, 2007;Kaifu et al, 2008) and Mooney et al (Mooney et al, 2010;Mooney et al, 2012) used octopus and squid species. Yet, Packard et al (Packard et al, 1990) used classical conditioning to address S. officinalis sound detection, and response thresholds were still two orders of magnitude higher than here.…”

Section: Discussion Acoustic Frequency Range and Sensitivitymentioning

confidence: 89%

“…Consequently, for vertebrates, sound detection is considered a primary sensory modality and an important component of vital intraspecific interactions and a key way to detect the surrounding environment. The ability of marine invertebrates to detect and potentially use sound is far less understood (Budelmann, 1992a;Budelmann, 1992b;Mooney et al, 2012). This is somewhat surprising given their relative abundance and central role in many marine ecosystems.…”

Section: Introductionmentioning

confidence: 99%

Graded behavioral responses and habituation to sound in the common cuttlefish, Sepia officinalis

Samson

Mooney

Gussekloo

et al. 2014

Journal of Experimental Biology

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Sound is a widely available and vital cue in aquatic environments, yet most bioacoustic research has focused on marine vertebrates, leaving sound detection in invertebrates poorly understood. Cephalopods are an ecologically key taxon that likely use sound and may be impacted by increasing anthropogenic ocean noise, but little is known regarding their behavioral responses or adaptations to sound stimuli. These experiments identify the acoustic range and levels that elicit a wide range of secondary defense behaviors such as inking, jetting and rapid coloration change. Secondarily, it was found that cuttlefish habituate to certain sound stimuli. The present study examined the behavioral responses of 22 cuttlefish (Sepia officinalis) to pure-tone pips ranging from 80 to 1000 Hz with sound pressure levels of 85-188 dB re. 1 μPa rms and particle accelerations of 0-17.1 m s −2 . Cuttlefish escape responses (inking, jetting) were observed between frequencies of 80 and 300 Hz and at sound levels above 140 dB re. 1 μPa rms and 0.01 m s −2 (0.74 m s −2 for inking responses). Body patterning changes and fin movements were observed at all frequencies and sound levels. Response intensity was dependent upon stimulus amplitude and frequency, suggesting that cuttlefish also possess loudness perception with a maximum sensitivity around 150 Hz. Cuttlefish habituated to repeated 200 Hz tone pips, at two sound intensities. Total response inhibition was not reached, however, and a basal response remained present in most animals. The graded responses provide a loudness sensitivity curve and suggest an ecological function for sound use in cephalopods.

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