Kelly S. Boyle

Sound production and spectral hearing sensitivity in the Hawaiian sergeant damselfish, Abudefduf abdominalis.

SUMMARY Sounds provide important signals for inter- and intraspecific communication in fishes, but few studies examine fish acoustic behavior in the context of coevolution of sound production and hearing ability within a species. This study characterizes the acoustic behavior in a reproductive population of the Hawaiian sergeant fish, Abudefduf abdominalis, and compares acoustic features to hearing ability, measured by the auditory evoked potential (AEP) technique. Sergeant fish produce sounds at close distances to the intended receiver (⩽1–2 body lengths), with different pulse characteristics that are associated primarily with aggression, nest preparation and courtship–female-visit behaviors. Energy peaks of all sounds were between 90 and 380 Hz, whereas courtship–visit sounds had a pulse repetition rate of 125 Hz with harmonic intervals up to 1 kHz. AEP threshold, which is probably higher than the behavioral threshold, indicates best sensitivity at low frequencies (95–240 Hz), with the lowest threshold at 125 Hz (123–127 dBrms re: 1 μPa). Thus, sound production and hearing in A. abdominalis are closely matched in the frequency domain and are useful for courtship and mating at close distances. Measured hearing thresholds did not differ among males and females during spawning or non-spawning periods, which indicates a lack of sex differences and seasonal variation in hearing capabilities. These data provide the first evidence that Abudefduf uses true acoustic communication on a level similar to that of both more derived (e.g. Dascyllus, Chromis) and more basal (e.g. Stegastes) soniferous pomacentrids. This correlation between sound production and hearing ability is consistent with the sensory drive model of signal evolution in which the sender and receiver systems coevolve within the constraints of the environment to maximize information transfer of acoustic signals.

Sexual dimorphism of sonic apparatus and extreme intersexual variation of sounds in Ophidion rochei (Ophidiidae): first evidence of a tight relationship between morphology and sound characteristics in Ophidiidae

BackgroundMany Ophidiidae are active in dark environments and display complex sonic apparatus morphologies. However, sound recordings are scarce and little is known about acoustic communication in this family. This paper focuses on Ophidion rochei which is known to display an important sexual dimorphism in swimbladder and anterior skeleton. The aims of this study were to compare the sound producing morphology, and the resulting sounds in juveniles, females and males of O. rochei.ResultsMales, females, and juveniles possessed different morphotypes. Females and juveniles contrasted with males because they possessed dramatic differences in morphology of their sonic muscles, swimbladder, supraoccipital crest, and first vertebrae and associated ribs. Further, they lacked the ‘rocker bone’ typically found in males. Sounds from each morphotype were highly divergent. Males generally produced non harmonic, multiple-pulsed sounds that lasted for several seconds (3.5 ± 1.3 s) with a pulse period of ca. 100 ms. Juvenile and female sounds were recorded for the first time in ophidiids. Female sounds were harmonic, had shorter pulse period (±3.7 ms), and never exceeded a few dozen milliseconds (18 ± 11 ms). Moreover, unlike male sounds, female sounds did not have alternating long and short pulse periods. Juvenile sounds were weaker but appear to be similar to female sounds.ConclusionsAlthough it is not possible to distinguish externally male from female in O. rochei, they show a sonic apparatus and sounds that are dramatically different. This difference is likely due to their nocturnal habits that may have favored the evolution of internal secondary sexual characters that help to distinguish males from females and that could facilitate mate choice by females. Moreover, the comparison of different morphotypes in this study shows that these morphological differences result from a peramorphosis that takes place during the development of the gonads.

Sound production mechanism in Gobius paganellus (Gobiidae)

SUMMARY Gobiidae, the largest fish family (>1500 species), has species from at least 10 genera that produce sounds for communication. Studies focused on goby sound production mechanisms have suggested that sounds are produced by the forcible ejection of water through small apertures in the opercles (hydrodynamic mechanism). The present study was a multidisciplinary investigation (morphology, muscle histology, high-speed video, sound analysis and electromyography) of the sound emission mechanism in Gobius paganellus, which produces both pulsed and tonal calls. Two populations were used, from Brittany and Venice. In the French population, sounds were accompanied by a suite of coordinated movements of the buccal, branchial and opercular regions. This was not the case in the Venetian population, and thus the direct role of head movements in sound production was rejected. The hydrodynamic mechanism hypothesis was also rejected in G. paganellus on the basis of sound oscillogram shape and because sounds are still produced after the opercles and hyohyoid muscles are cut. The use of both electromyography and electron microscopy showed that the levator pectoralis muscle, which originates on the skull and inserts on the dorsal tip of the cleithrum, is involved in sound production. We propose that the contraction of this muscle and associated vibration of the large radials is used to make sounds. In addition, we propose that different sound types (pulsed sounds and tonal calls) could occur because of differences in fish size.

Pulse sound generation, anterior swim bladder buckling and associated muscle activity in the pyramid butterflyfish, Hemitaurichthys polylepis

SUMMARY Acoustic behaviors are widespread among diverse fish taxa but mechanisms of sound production are known from relatively few species, vary widely and convergent mechanisms are poorly known. We examined the sound production mechanism in the pyramid butterflyfish, Hemitaurichthys polylepis, a member of the socially and ecologically diverse reef fish family Chaetodontidae. In the field, fish produce pulse trains at dusk during social interactions that are probably related to mate attraction and courtship. In laboratory experiments, sound production was synchronized to high-speed video to determine body movement associated with sound generation. In addition, electromyography (EMG) recordings tested the activity of six candidate muscles. Fish produced individual pulses with a mean peak frequency of 97 Hz in rapid succession. EMG experiments show that anterior hypaxial muscles contract at high bilaterally synchronous rates (up to 120 Hz) in near perfect association with rapid inward buckling visible outside the body over the anterior swim bladder. Muscle activity often showed EMG doublets that occurred within the time of a single sound pulse but was not sustained. Buckling and sound pulse rates correlated strongly (R2≈1.00) and sound pulse rate measured over two successive pulses (maximum of 38 pulses s–1) was lower than muscle firing rate. These results show that the extrinsic swim bladder muscles of pyramid butterflyfish involve single contractions that produce pulses in a manner similar to distantly related teleosts, but involve a novel doublet motor-neuron firing pattern. Thus, the sound production mechanism in pyramid butterflyfish is likely convergent with several percomorph taxa and divergent from the related chaetodontid genus Forcipiger.

Modifications in Call Characteristics and Sonic Apparatus Morphology During Puberty in Ophidion rochei (Actinopterygii: Ophidiidae)

Juveniles, females, and males of Ophidion rochei share similar external morphology, probably because they are mainly active in the dark, which reduces the role of visual cues. Their internal sonic apparatuses, however, are complex: three pairs of sonic muscles, and highly modified vertebrae and ribs are involved in sound production. The sonic apparatus of males differs from juveniles and females in having larger swimbladder plates (modified ribs associate with the swimbladder wall) and sonic muscles, a modified swimbladder shape and a mineralized structure called the “rocker bone” in front of the swimbladder. All of these male traits appear at the onset of sexual maturation. This article investigates the relationship between morphology and sounds in male O. rochei of different sizes. Despite their small size range total length (133–170 mm TL), the five specimens showed pronounced differences in sound‐production apparatus morphology, especially in terms of swimbladder shape and rocker bone development. This observation was reinforced by the positive allometry measured for the rocker bone and the internal tube of the swimbladder. The differences in morphology were related to marked differences in sound characteristics (especially frequency and pulse duration). These results suggest that male calls carry information about the degree of maturity. Deprived of most visual cues, ophidiids probably have invested in other mechanisms to recognize and distinguish among individual conspecifics and between ophidiid species. As a result, their phenotypes are externally similar but internally very different. In these taxa, the great variability of the sound production apparatus means this complex system is a main target of environmental constraints. J. Morphol. 275:650–660, 2014.

Sound production and mechanism in Heniochus chrysostomus (Chaetodontidae)

SUMMARY The diversity in calls and sonic mechanisms appears to be important in Chaetodontidae. Calls in Chaetodon multicinctus seem to include tail slap, jump, pelvic fin flick and dorsal–anal fin erection behaviors. Pulsatile sounds are associated with dorsal elevation of the head, anterior extension of the ventral pectoral girdle and dorsal elevation of the caudal skeleton in Forcipiger flavissiumus. In Hemitaurichthys polylepis, extrinsic swimbladder muscles could be involved in sounds originating from the swimbladder and correspond to the inward buckling of tissues situated dorsally in front of the swimbladder. These examples suggest that this mode of communication could be present in other members of the family. Sounds made by the pennant bannerfish (Heniochus chrysostomus) were recorded for the first time on coral reefs and when fish were hand held. In hand-held fishes, three types of calls were recorded: isolated pulses (51%), trains of four to 11 pulses (19%) and trains preceded by an isolated pulse (29%). Call frequencies were harmonic and had a fundamental frequency between 130 and 180 Hz. The fundamental frequency, sound amplitude and sound duration were not related to fish size. Data from morphology, sound analysis and electromyography recordings highlight that the calls are made by extrinsic sonic drumming muscles in association with the articulated bones of the ribcage. The pennant bannerfish system differs from other Chaetodontidae in terms of sound characteristics, associated body movements and, consequently, mechanism.

Sound production in the longnose butterflyfishes (genus Forcipiger): cranial kinematics, muscle activity and honest signals

SUMMARY Many teleost fishes produce sounds for social communication with mechanisms that do not involve swim bladder musculature. Such sounds may reflect physical attributes of the sound-production mechanism, be constrained by body size and therefore control signal reliability during agonistic behaviors. We examined kinematics of the cranium, median fins and caudal peduncle during sound production in two territorial chaetodontid butterflyfish sister species: forcepsfish (Forcipiger flavissimus) and longnose butterflyfish (F. longirostris). During intraspecific agonistic encounters, both species emit a single pulse sound that precedes rapid cranial rotation at velocities and accelerations that exceed those of prey strikes by many ram-and suction-feeding fishes. Electromyography showed that onsets of activity for anterior epaxialis, sternohyoideus, A1 and A2 adductor mandibulae muscles and sound emission are coincident but precede cranial elevation. Observations indicate that sound production is driven by epaxial muscle contraction whereas a ventral linkage between the head and pectoral girdle is maintained by simultaneous activity from the adductor mandibulae and sternohyoideus. Thus, the girdle, ribs and rostral swim bladder are pulled anteriorly before the head is released and rotated dorsally. Predictions of the hypothesis that acoustic signals are indicators of body size and kinematic performance were confirmed. Variation in forcepsfish sound duration and sound pressure level is explained partly by cranial elevation velocity and epaxial electromyogram duration. Body size, however, explains most variation in duration and sound pressure level. These observed associations indicate that forcepsfish sounds may be accurate indicators of size and condition that are related to resource holding potential during social encounters.

Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae)

Elucidating the origins of complex biological structures has been one of the major challenges of evolutionary studies. Within vertebrates, the capacity to produce regular coordinated electric organ discharges (EODs) has evolved independently in different fish lineages. Intermediate stages, however, are not known. We show that, within a single catfish genus, some species are able to produce sounds, electric discharges or both signals (though not simultaneously). We highlight that both acoustic and electric communication result from actions of the same muscle. In parallel to their abilities, the studied species show different degrees of myofibril development in the sonic and electric muscle. The lowest myofibril density was observed in Synodontis nigriventris, which produced EODs but no swim bladder sounds, whereas the greatest myofibril density was observed in Synodontis grandiops, the species that produced the longest sound trains but did not emit EODs. Additionally, S. grandiops exhibited the lowest auditory thresholds. Swim bladder sounds were similar among species, while EODs were distinctive at the species level. We hypothesize that communication with conspecifics favoured the development of species-specific EOD signals and suggest an evolutionary explanation for the transition from a fast sonic muscle to electrocytes.

A superfast muscle in the complex sonic apparatus of Ophidion rochei (Ophidiiformes): histological and physiological approaches

In teleosts, superfast muscles are generally associated with the swimbladder wall, whose vibrations result in sound production. In Ophidion rochei, three pairs of muscles were named ‘sonic’ because their contractions affect swimbladder position: the dorsal sonic muscle (DSM), the intermediate sonic muscle (ISM), and the ventral sonic muscle (VSM). These muscles were investigated thanks to electron microscopy and electromyography in order to determine their function in sound production. Fibers of the VSM and DSM were much thinner than the fibers of the ISM and epaxial musculature. However, only VSM fibers had the typical ultrastructure of superfast muscles: low proportion of myofibrils, and high proportions of sarcoplasmic reticulum and mitochondria. In females, each sound onset was preceded by the onset of electrical activity in the VSM and the DSM (ISM was not tested). The electromyograms of the VSM were very similar to the waveforms of the sounds: means for the pulse period were 3.6±0.5 and 3.6±0.7 ms, respectively. This shows that the fast VSM (ca. 280 Hz) is responsible for the pulse period and fundamental frequency of female sounds. DSM electromyograms were generally characterized by one or two main peaks followed by periods of lower electrical activity, which suggests a sustained contraction over the course of the sound. The fiber morphology of the ISM and its antagonistic position relative to the DSM are not indicative of a muscle capable of superfast contractions. Overall, this study experimentally shows the complexity of the sound production mechanism in the nocturnal fish O. rochei.

Fast drum strokes: novel and convergent features of sonic muscle ultrastructure, innervation, and motor neuron organization in the Pyramid Butterflyfish (Hemitaurichthys polylepis).

Sound production that is mediated by intrinsic or extrinsic swim bladder musculature has evolved multiple times in teleost fishes. Sonic muscles must contract rapidly and synchronously to compress the gas‐filled bladder with sufficient velocity to produce sound. Muscle modifications that may promote rapid contraction include small fiber diameter, elaborate sarcoplasmic reticulum (SR), triads at the A–I boundary, and cores of sarcoplasm. The diversity of innervation patterns indicate that sonic muscles have independently evolved from different trunk muscle precursors. The analysis of sonic motor pathways in distantly related fishes is required to determine the relationships between sonic muscle evolution and function in acoustic signaling. We examined the ultrastructure of sonic and adjacent hypaxial muscle fibers and the distribution of sonic motor neurons in the coral reef Pyramid Butterflyfish (Chaetodontidae: Hemitaurichthys polylepis) that produces sound by contraction of extrinsic sonic muscles near the anterior swim bladder. Relative to adjacent hypaxial fibers, sonic muscle fibers were sparsely arranged among the endomysium, smaller in cross‐section, had longer sarcomeres, a more elaborate SR, wider t‐tubules, and more radially arranged myofibrils. Both sonic and non‐sonic muscle fibers possessed triads at the Z‐line, lacked sarcoplasmic cores, and had mitochondria among the myofibrils and concentrated within the peripheral sarcoplasm. Sonic muscles of this derived eutelost possess features convergent with other distant vocal taxa (other euteleosts and non‐euteleosts): small fiber diameter, a well‐developed SR, and radial myofibrils. In contrast with some sonic fishes, however, Pyramid Butterflyfish sonic muscles lack sarcoplasmic cores and A–I triads. Retrograde nerve label experiments show that sonic muscle is innervated by central and ventrolateral motor neurons associated with spinal nerves 1–3. This restricted distribution of sonic motor neurons in the spinal cord differs from many euteleosts and likely reflects the embryological origin of sonic muscles from hypaxial trunk precursors rather than occipital somites. J. Morphol., 2013.