New insights into the role of the pharyngeal jaw apparatus in the sound-producing mechanism of <i>Haemulon flavolineatum</i> (Haemulidae)

Bertucci, Frédéric; Ruppé, Laëtitia; Wassenbergh, Sam Van; Compère, Philippe; Parmentier, Éric

doi:10.1242/jeb.109025

Cited by 20 publications

(13 citation statements)

References 53 publications

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“…Quantitative comparisons indicate the same sounds are produced during food processing as in distress situations. Videos showed cyclic movements during sound production were similar to movements employed in food processing, and electron microscopy revealed traces of erosion on different teeth of the pharyngeal jaws (Bertucci et al ., ).…”

Section: The Concept Of Exaptationmentioning

confidence: 97%

“…Rubbing of upper and lower pharyngeal teeth produces stridulatory sounds (Burkenroad, 1930;Moulton, 1958). Bertucci et al (2014) performed a study on the French grunt (Haemulon flavolineatum, Haemulidae) using hydrophones to record sounds, high-speed X ray videos (to see bone movements inside the buccal cavity) and electron microscopy to study the teeth of the pharyngeal jaws was realized. Quantitative comparisons indicate the same sounds are produced during food processing as in distress situations.…”

Section: Haemulidae: Sound Production From Pharyngeal Jawsmentioning

confidence: 99%

“…Producing sound involves a vibration coupled to the medium (Bradbury & Vehrencamp, ). Five basic mechanisms have been documented in teleost communication: (i) muscular vibrations of a membrane or sac (Fine, King, & Cameron, ; Millot, Vandewalle, & Parmentier, ), (ii) stridulation (Bertucci, Ruppé, Wassenbergh, Compère, & Parmentier, ; Fine, King, Friel, Loesser, & Newton, ; Parmentier et al ., ), (iii) forced flow through a small orifice (Fish & Mowbray, ; Lagardère & Ernande, ; Wahlberg & Westerberg, ; Wilson, Batty, & Dill, ), (iv) muscular vibration of appendages (Colleye, Ovidio, Salmon, & Parmentier, ; Ladich, ; Parmentier et al ., ) and (v) percussion on a substrate (Colleye et al ., ). Moreover, although multiple submechanisms have been described, most fall into two categories: (i) muscles that directly or indirectly insert on the swim bladder and (ii) stridulatory mechanisms involving the rubbing of bones.…”

Section: Introductionmentioning

confidence: 99%

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Multiple exaptations leading to fish sound production

2017

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The term exaptation introduced by Stephen J. Gould and Elizabeth Vrba has been used infrequently. The high diversity of sound‐producing mechanisms in fishes highlights a recurrent use of this process in unrelated taxa. We propose that sonic evolution typically involves exaptations: in many fish taxa, sound production was acquired by the independent modification of existing structures with other functions. These structures were modified into complex effectors for courtship and agonistic sound production without major changes to their gnathostome Bauplan. Existing anatomical structures (teeth, bones, etc.) were likely first used in non‐voluntary sound production, which incidentally provided advantages and could then be selected specifically for signal production leading to the refinement of more sophisticated sonic organs. We postulate that in many if not most cases, sound‐production specializations originated in fish taxa that took advantage of incidental non‐voluntary sounds. We use different case‐studies to show that exaptation may be a key, albeit largely unrecognized, agent of major morphological and behavioural changes.

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Section: The Concept Of Exaptationmentioning

confidence: 97%

Section: Haemulidae: Sound Production From Pharyngeal Jawsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Multiple exaptations leading to fish sound production

2017

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“…Obviously, this work should be repeated with modern physiological and acoustic tools. A recent study using X-ray videos has conclusively demonstrated sound pulses generated by rubbing pharyngeal teeth in the French grunt Haemulon flavolineatum (Bertucci et al 2014).…”

Section: Stridulation Mechanismsmentioning

confidence: 99%

Mechanisms of Fish Sound Production

Fine

Parmentier

2015

Animal Signals and Communication

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Fishes have evolved multiple mechanisms for sound production, many of which utilize sonic muscles that vibrate the swimbladder or the rubbing of bony elements. Sonic muscles are among the fastest muscles in vertebrates and typically drive the swimbladder to produce one sound cycle per contraction. These muscles may be extrinsic, typically extending from the head to the swimbladder, or intrinsic, likely a more-derived condition, in which muscles attach exclusively to the bladder wall. Recently discovered in Ophidiiform fishes, slow muscles stretch the swimbladder and associated tendons, allowing sound production by rebound (cock and release). In glaucosomatids, fast muscles produce a weak sound followed by a louder one, again produced by rebound, which may reflect an intermediate in the evolution of slow to superfast sonic muscles. Historically, the swimbladder has been modeled as an underwater resonant bubble. We provide evidence for an alternative hypothesis, namely that bladder sounds are driven as a forced rather than a resonant response, thus accounting for broad tuning, rapid damping, and directionality of fish sounds. Cases of sounds that damp slowly, an indication of resonance, are associated with tendons or bones that continue to vibrate and hence drive multiple cycles of swimbladder sound. Stridulation sounds, best studied in catfishes and damselfishes, are produced, respectively, as a series of quick jerks causing rubbing of a ribbed process against a rough surface or rapid jaw closing mediated by a specialized tendon. A cladogram of sonic fishes suggests that fish sound production has arisen independently multiple times.

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“…In some cases, a secondary swim bladder function has evolved that enables these species of fish to produce sound for acoustic communication (Fine & Parmentier, 2015;Kasumyan, 2008;Parmentier & Diogo, 2006). In grunts (Haemulidae) and clownfishes (Pomacentridae), the swim bladder acts as an acoustic amplifier to increase the sound level produced by the stridulation of hard skeletal parts including vibrations of the rib cage driven by jaw snapping (Bertucci, Ruppe, Van Wassenbergh, Compere, & Parmentier, 2014;Colleye, Nakamura, Fr ed erich, & Parmentier, 2012;Parmentier et al, 2007). In toadfishes and midshipman (Batrachoididae), sound is produced predominantly by reproductive males that have enlarged sonic muscles attached to their swim bladders and when contracted vibrate the bladder to yield high sound level acoustic signals for social communication (Bass & McKibben, 2003;Fine, Burns, & Harris, 1990;Fine, Bernard, & Harris, 1993;Fine, Malloy, King, Mitchell, & Cameron, 2001;Fine & Parmentier, 2015).…”

Section: Introductionmentioning

confidence: 99%

Intra‐ and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection

Mohr

Whitchurch

Anderson

et al. 2017

Journal of Morphology

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The plainfin midshipman fish, Porichthys notatus, is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra- and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro-computerized tomography revealed that females and type II males have prominent, horn-like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner-ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.

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New insights into the role of the pharyngeal jaw apparatus in the sound-producing mechanism of Haemulon flavolineatum (Haemulidae)

Cited by 20 publications

References 53 publications

Multiple exaptations leading to fish sound production

Multiple exaptations leading to fish sound production

Mechanisms of Fish Sound Production

Intra‐ and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection

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