Ontogeny of Acoustic and Feeding Behaviour in the Grey Gurnard, Eutrigla gurnardus

Although sound production in teleost fish is often associated with territorial behaviour, little is known of fish acoustic behaviour in other agonistic contexts such as competitive feeding and how it changes during ontogeny. The grey gurnard, Eutrigla gurnardus, frequently emits knock and grunt sounds during competitive feeding and seems to adopt both contest and scramble tactics under defensible resource conditions. Here we examine, for the first time, the effect of fish size on sound production and agonistic behaviour during competitive feeding. We have made sound (alone) and video (synchronized image and sound) recordings of grey gurnards during competitive feeding interactions. Experimental fish ranged from small juveniles to large adults and were grouped in four size classes: 10–15, 15–20, 25–30 and 30–40 cm in total length. We show that, in this species, both sound production and feeding behaviour change with fish size. Sound production rate decreased in larger fish. Sound duration, pulse duration and the number of pulses increased whereas the peak frequency decreased with fish size, in both sound types (knocks and grunts). Interaction rate and the frequency of agonistic behaviour decreased with increasing fish size during competitive feeding sessions. The proportion of feeding interactions accompanied by sound production was similar in all size classes. However, the proportion of interactions accompanied by knocks (less aggressive sounds) and by grunts (more aggressive) increased and decreased with fish size, respectively. Taken together, these results suggest that smaller grey gurnards compete for food by contest tactics whereas larger specimens predominantly scramble for food, probably because body size gives an advantage in locating, capturing and handling prey. We further suggest that sounds emitted during feeding may potentially give information on the motivation and ability of the individual to compete for food resources.     

Learned or innate production of acoustic signals in fishes: a test using a cyprinid

No information on the inheritance of the ability to produce sounds exists for fishes. In birds, which usually provide extensive post-hatching parental care, acoustic signals are learned in some species but are innate in others. Almost no fishes provide extensive post-hatching parental care and, consequently, the offspring have little opportunity to hear and learn sounds produced by the parents (usually the male in fishes); they may, however, be exposed to acoustic signals of conspecifics in the same habitat. We used a cyprinid, Codoma ornata, to test whether sound production is learned from the parents or whether it is innate. Fertilized eggs of this species were raised in isolation from adults. Upon maturity, these fish were tested for sound production in aggressive and reproductive contexts. Fish which had no contact with adults, and therefore no opportunity to hear the acoustic signals of their species, produced sounds that were similar to those produced by their parents, and they produced these in the same contexts. Significant differences were observed in dominant frequency for one context, with the smaller F₁ fish having signals of higher frequency than parental fish. Since no opportunity for learning existed, this provided evidence that the ability to produce sounds is innate in this minnow species.     

Production of acoustic signals during aggression in Coosa bass, <Emphasis Type="Italic">Micropterus coosae</Emphasis>

Although sound production has been described for sunfishes, it is previously unknown for basses, both groups of fishes in the family Centrarchidae. We document production of acoustic signals during aggressive encounters in Coosa bass, Micropterus coosae. During dyadic encounters, presumptive winners of contests produced sounds associated with a variety of behaviors, including chases, lateral displays, circle swims, nudging, jerking and during post aggression, while fish were stationary. These sounds are low-frequency, non-harmonic and consist of one to 41 separate pulses. In most trials larger fish won contests, regardless of territory ownership (which fish was put into the test tank first) and size difference.     

Sounds Modulate Males’ Aggressiveness in a Cichlid Fish

Acoustic signals are produced in many fish species during agonistic or courtship interactions. A way to test the biological role of these sounds is the use of acoustic playback experiments. However, sounds are usually associated with visual displays and playback experiments performed in fish so far, often failed to match acoustic and visual stimuli. To avoid this mismatch issue, we experimentally separated or coupled visual and acoustic channels to test the role of sounds produced during male–male aggressive interactions in a cichlid fish, Metriaclima zebra. Results show that aggressive behaviour is based on visual stimuli and that acoustic signals alone never trigger aggression. Furthermore, the association between visual and acoustic channels lowers the level of aggressiveness found when fish can only interact visually. This suggests that acoustic signals used during a dispute may complement visual displays to modulate males’ behaviour by reducing their aggressiveness and the risk of escalated fights.     

Acoustic signalling in female fish: factors influencing sound characteristics in croaking gouramis

The characteristics of sounds produced by fishes are influenced by several factors such as size. The current study analyses factors affecting structural properties of acoustic signals produced by female croaking gouramis Trichopsis vittata during agonistic interactions. Female sounds (although seldom analysed separately from male sounds) can equally be used to investigate factors affecting the sound characteristics in fish. Sound structure, dominant frequency and sound pressure levels (SPL) were determined and correlated to body size and the order in which sounds were emitted. Croaking sounds consisted of series of single-pulsed or double-pulsed bursts, each burst produced by one pectoral fin. Main energies were concentrated between 1.3 and 1.5 kHz. The dominant frequency decreased with size, as did the percentage of single-pulsed bursts within croaking sounds. The SPL and the number of bursts within a sound were independent of size but decreased significantly with the order of their production. Thus, acoustic signals produced at the beginning of agonistic interactions were louder and consisted of more bursts than subsequent ones. Our data indicate that body size affects the dominant frequency and structure of sounds. The increase in the percentage of double-pulsed bursts with size may be due to stronger pectoral muscles in larger fish. In contrast, ongoing fights apparently result in muscle fatigue and subsequently in a decline in the number of bursts and SPL. The factor ‘order of sound production’ points to an intra-individual variability of sounds and should be considered in future studies.     

First attempt to use a remotely operated vehicle to observe soniferous fish behavior in the Gulf of Maine, Western Atlantic Ocean

Underwater sound and video observations were made at noon, sunset, and midnight in sand, gravel, and boulder habitat in the Stellwagen Bank National Marine Sanctuary, Gulf of Maine, USA in October 2001 using a remotely operated vehicle (ROV). Seventeen species of fish and squid were observed with clear habitat and time differences. Observations of feeding behavior, disturbance behavior, and both interspecific and intraspecific interactions provided numerous opportunities for potential sound production; however, sounds were recorded only during a single dive. Although high noise levels generated by the ROV and support ship may have masked some sounds, we conclude that fish sound production in the Gulf of Maine during the fall is uncommon. The recorded fish sounds are tentatively attributed to the cusk Brosme brosme. Cusk sounds consisted variously of isolated thumps, widely spaced thump trains, drumrolls, and their combinations. Frequency peaks were observed at 188, 539, and 1195 Hz. Use of a remotely operated vehicle (ROV) as a passive acoustic observation platform was problematic due to high ROV self-noise and the ROV's inability to maintain a fixed position on the bottom without thruster power. Some fishes were clearly also disturbed by ROV noise, indicating a potential ROV sampling bias. Based on our observations, we suggest that new instruments incorporating both optic and passive acoustic technologies are needed to provide better tools for in situ behavioral studies of cusk and other fishes [Current Zoology 56 (1): 90-99 2010].     

Sound production and reproductive behaviour of the armoured catfish Corydoras paleatus (Callichthyidae)

Sound production during reproductive behaviour, dyadic encounters and distress situations was investigated in the callichthyid catfish Corydoras paleatus. Sounds were broad-band, pulsed, acoustic signals produced during abduction of the pectoral spines. Only males emitted trains of sounds during courting and trains of sounds of shorter duration during dyadic encounters. Several males, which are usually smaller than females, courted one gravid female without obvious cooperation or competition between them. During mating, one previously vocalizing male clasped the female's barbels with one pectoral spine and inseminated the eggs. The number of successful spawnings, days until spawning, and number of eggs laid was not related to the number of males (one, two or three) combined with one female. Males did not behave aggressively towards each other during courting or in dyadic encounters. In distress situations, when fish were hand held, both sexes and juveniles produced single sounds. The dominant frequency was negatively correlated with body size and the sound duration was positively correlated with relative length of pectoral spines (standardized to body length). This acoustical behaviour in C. paleatus differs considerably from Hoplosternum thoracatum, a representative of the callichthyine subfamily, in which vocalization was observed during territorial behaviour in males and aggressive behaviour in both sexes. This is the first report of a major difference in vocalizing behaviour within one teleost family.     

Sex-Specific Differences in Agonistic Behaviour,Sound Production and Auditory Sensitivity in the Callichthyid Armoured Catfish Megalechis thoracata

Background

Data on sex-specific differences in sound production, acoustic behaviour and hearing abilities in fishes are rare. Representatives of numerous catfish families are known to produce sounds in agonistic contexts (intraspecific aggression and interspecific disturbance situations) using their pectoral fins. The present study investigates differences in agonistic behaviour, sound production and hearing abilities in males and females of a callichthyid catfish.

Methodology/Principal Findings

Eight males and nine females of the armoured catfish Megalechis thoracata were investigated. Agonistic behaviour displayed during male-male and female-female dyadic contests and sounds emitted were recorded, sound characteristics analysed and hearing thresholds measured using the auditory evoked potential (AEP) recording technique. Male pectoral spines were on average 1.7-fold longer than those of same-sized females. Visual and acoustic threat displays differed between sexes. Males produced low-frequency harmonic barks at longer distances and thumps at close distances, whereas females emitted broad-band pulsed crackles when close to each other. Female aggressive sounds were significantly shorter than those of males (167 ms versus 219 to 240 ms) and of higher dominant frequency (562 Hz versus 132 to 403 Hz). Sound duration and sound level were positively correlated with body and pectoral spine length, but dominant frequency was inversely correlated only to spine length. Both sexes showed a similar U-shaped hearing curve with lowest thresholds between 0.2 and 1 kHz and a drop in sensitivity above 1 kHz. The main energies of sounds were located at the most sensitive frequencies.

Conclusions/Significance

Current data demonstrate that both male and female M. thoracata produce aggressive sounds, but the behavioural contexts and sound characteristics differ between sexes. Sexes do not differ in hearing, but it remains to be clarified if this is a general pattern among fish. This is the first study to describe sex-specific differences in agonistic behaviour in fishes.     

First evidence of fish larvae producing sounds

The acoustic ecology of marine fishes has traditionally focused on adults, while overlooking the early life-history stages. Here, we document the first acoustic recordings of pre-settlement stage grey snapper larvae (Lutjanus griseus). Through a combination of in situ and unprovoked laboratory recordings, we found that L. griseus larvae are acoustically active during the night, producing ‘knock’ and ‘growl’ sounds that are spectrally and temporally similar to those of adults. While the exact function and physiological mechanisms of sound production in fish larvae are unknown, we suggest that these sounds may enable snapper larvae to maintain group cohesion at night when visual cues are reduced.     

Sounds and sound production in fishes

The main information on the sounds and sound production in fishes is reviewed. The present systems of sound classification and specialized sound production in fishes with different taxonomic positions and ecology are described. The anatomy of sound generating organs is analyzed, and the mechanisms of production of different types of sounds (stridulation, drumming, cavitation, and percussion, as well as hydrodynamic, pneumatic, stringed, and respiratory sounds) are discussed. A brief characterization of the acoustic parameters of different sound types is given. Recent data on the anatomy and morphology of the sonic muscles (including their innervation, physiology, sexual dimorphism, and seasonal changes) are reviewed. The dynamics of the development of sound generating organs are described, and their capacity for sound production in the ontogeny of fishes is followed.     

Four type of sounds for one winner: vocalizations during territorial behavior in the red-mouthed goby <Emphasis Type="Italic">Gobius cruentatus</Emphasis> (Pisces Gobiidae)

During territorial encounters, the acoustic repertoire of Gobius cruentatus consists of four types of sound emissions: a tonal sound, a noisy tonal sound, a train of individual pulses, and a complex sound. The complex sound is made of two distinct elements, an initial tonal part followed by pulses. This is the largest acoustic repertoire described so far in gobiid fish during aggressive interaction. Sounds are emitted, mainly by the residents, when fish have already started the interaction but before the encounter is settled. Therefore, sounds seem to have a threatening function.     

Behaviours Associated with Acoustic Communication in Nile Tilapia (Oreochromis niloticus)

Background

Sound production is widespread among fishes and accompanies many social interactions. The literature reports twenty-nine cichlid species known to produce sounds during aggressive and courtship displays, but the precise range in behavioural contexts is unclear. This study aims to describe the various Oreochromis niloticus behaviours that are associated with sound production in order to delimit the role of sound during different activities, including agonistic behaviours, pit activities, and reproduction and parental care by males and females of the species.

Methodology/Principal Findings

Sounds mostly occur during the day. The sounds recorded during this study accompany previously known behaviours, and no particular behaviour is systematically associated with sound production. Males and females make sounds during territorial defence but not during courtship and mating. Sounds support visual behaviours but are not used alone. During agonistic interactions, a calling Oreochromis niloticus does not bite after producing sounds, and more sounds are produced in defence of territory than for dominating individuals. Females produce sounds to defend eggs but not larvae.

Conclusion/Significance

Sounds are produced to reinforce visual behaviours. Moreover, comparisons with O. mossambicus indicate two sister species can differ in their use of sound, their acoustic characteristics, and the function of sound production. These findings support the role of sounds in differentiating species and promoting speciation. They also make clear that the association of sounds with specific life-cycle roles cannot be generalized to the entire taxa.     

Geographical variation in sound production in the anemonefish Amphiprion akallopisos

Because of pelagic-larval dispersal, coral-reef fishes are distributed widely with minimal genetic differentiation between populations. Amphiprion akallopisos, a clownfish that uses sound production to defend its anemone territory, has a wide but disjunct distribution in the Indian Ocean. We compared sounds produced by these fishes from populations in Madagascar and Indonesia, a distance of 6500 km. Differentiation of agonistic calls into distinct types indicates a complexity not previously recorded in fishes' acoustic communication. Moreover, various acoustic parameters, including peak frequency, pulse duration, number of peaks per pulse, differed between the two populations. The geographic comparison is the first to demonstrate 'dialects' in a marine fish species, and these differences in sound parameters suggest genetic divergence between these two populations. These results highlight the possible approach for investigating the role of sounds in fish behaviour in reproductive divergence and speciation.     

Acoustic behaviour of Abudefduf luridus

Adult males Abudefduf luridus produced sounds during aggressive interactions, although not all aggressive interactions were associated with sounds. Such sounds were always related to characteristic swimming movements during an aggressive display or territorial defence. The sound was a combination of several sonic pulses, with most energy concentrated towards the low end of the spectrum (from <50 to 800 Hz), and was most frequently groups of two pulses. Analysis of the pulse structure suggested that these sounds are produced by muscles acting on the swimbladder. However, the mechanism of sound production has yet to be demonstrated. Sounds were emitted throughout the 24-h period with increased activity at sunrise and sunset.     

Development of agonistic behaviour and vocalization in croaking gouramis

The development of agonistic behaviour and vocalization in the croaking gourami Trichopsis vittata was studied from hatching to sexual maturity (4 months of age). Initial interactions started when fry were 11 days old and consisted of approach and flight in a feeding context. More complex threat patterns appeared during dyadic encounters as fish grew older. Lateral display (spreading of median fins in a lateral position) first occurred during the third week, circling shortly afterwards and pectoral fin beating when fish were 7 weeks old. Rapid pectoral fin beating was first accompanied by sound emission at 8 weeks. Initially, croaking sounds were built up mainly of a series of single pulses, each one produced by one pectoral fin. Later, single pulses gave way to double pulses. Furthermore, pulse period and number of pulses increased, while the dominant frequency of croaks decreased significantly with age. After vocalization was established, frontal display, mouth biting and retreat behaviour occurred at the age of 10 weeks. Initially, young exhibited vertical bars which gave way to dots and horizontal bars at 8 weeks when fish started to vocalize. The order of appearance of behavioural patterns during ontogeny corresponds to the order of appearance in fights between adults. This is the first study demonstrating that the ontogenetic development of social signalling comprises characteristic changes in behaviour, vocalization and coloration in a teleost fish.     

Sound production during competitive feeding in the grey gurnard

The acoustic repertoire of captive grey gurnard Eutrigla gurnardus during competitive feeding consisted of three types of sound: knocks, grunts and growls. Knocks were audible as a single sound, whereas grunts and growls were perceived as longer, pulsed sounds to the human ear. Typically, knocks were composed of 1–2 pulses, grunts of 4–8 pulses and growls >10 pulses. Growls were longer and had shorter pulse periods than grunts. All sound types had peak frequencies of c . 500 Hz. The sequences of behaviours observed during feeding interactions suggest that grey gurnard obtain food both by scramble and contest tactics. Competing fish emitted knocks mainly while grasping a food item and also during other non‐agonistic behaviour, suggesting that knock production may reflect a state of feeding arousal but could also serve as a warning of the forager's presence to nearby competitors. Grunts were mainly emitted during frontal displays, which were the most frequent behavioural act preceding grasps, suggesting that they may play a role in deterring other fish from gaining access to disputed food items.     

An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes

Fishes use a variety of sensory systems to learn about their environments and to communicate. Of the various senses, hearing plays a particularly important role for fishes in providing information, often from great distances, from all around these animals. This information is in all three spatial dimensions, often overcoming the limitations of other senses such as vision, touch, taste and smell. Sound is used for communication between fishes, mating behaviour, the detection of prey and predators, orientation and migration and habitat selection. Thus, anything that interferes with the ability of a fish to detect and respond to biologically relevant sounds can decrease survival and fitness of individuals and populations. Since the onset of the Industrial Revolution, there has been a growing increase in the noise that humans put into the water. These anthropogenic sounds are from a wide range of sources that include shipping, sonars, construction activities (e.g., wind farms, harbours), trawling, dredging and exploration for oil and gas. Anthropogenic sounds may be sufficiently intense to result in death or mortal injury. However, anthropogenic sounds at lower levels may result in temporary hearing impairment, physiological changes including stress effects, changes in behaviour or the masking of biologically important sounds. The intent of this paper is to review the potential effects of anthropogenic sounds upon fishes, the potential consequences for populations and ecosystems and the need to develop sound exposure criteria and relevant regulations. However, assuming that many readers may not have a background in fish bioacoustics, the paper first provides information on underwater acoustics, with a focus on introducing the very important concept of particle motion, the primary acoustic stimulus for all fishes, including elasmobranchs. The paper then provides background material on fish hearing, sound production and acoustic behaviour. This is followed by an overview of what is known about effects of anthropogenic sounds on fishes and considers the current guidelines and criteria being used world-wide to assess potential effects on fishes. Most importantly, the paper provides the most complete summary of the effects of anthropogenic noise on fishes to date. It is also made clear that there are currently so many information gaps that it is almost impossible to reach clear conclusions on the nature and levels of anthropogenic sounds that have potential to cause changes in animal behaviour, or even result in physical harm. Further research is required on the responses of a range of fish species to different sound sources, under different conditions. There is a need both to examine the immediate effects of sound exposure and the longer-term effects, in terms of fitness and likely impacts upon populations.     

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles [1.9–3.1 cm standard length (SL), large juveniles (6.8–8.0 cm SL) and non-reproductive adults (9.0–22.6 cm SL)]. The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75–1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.     

The Role of Agonistic Sounds in Male Nest Defence in the Painted Goby Pomatoschistus pictus

Animals often vocalize during territorial challenges as acoustic signals may indicate motivation and fighting ability and contribute to reduce aggressive escalation. Here, we tested the function of agonistic sounds in territorial defence in the painted goby. Pomatoschistus pictus, a small vocal marine fish that defends nests during the breeding season. We first measured the number of times a male approached, avoided, explored, entered and exited two unattended nests associated with either conspecific agonistic sounds or a control: silence or white noise. Acoustic stimuli were played back when the male approached a nest. In a second experimental set, we added visual stimuli, consisting of a conspecific male in a small confinement aquarium near each nest. Even though we found no effect of the visual stimuli, the sound playbacks induced similar effects in both experimental conditions. In the sound vs. silence treatment, we found that when males approached a nest, the playback of conspecific sounds usually triggered avoidance. However, this behaviour did not last as in longer periods males visited nests associated with agonistic sounds more often than silent ones. When the control was white noise, we found no significant effect of the playback treatment in male behaviour. Although we cannot exclude the possibility that other sounds may dissuade nest occupation, our results suggest that agonistic sounds act as territorial intrusion deterrents but are insufficient to prevent nest intrusion on their own. Further studies are needed to test the significance of sound production rate, spectral content and temporal patterns to deter territorial intrusion in fish.     

Differences between male,female and juvenile haddock (Melanogrammus aeglefinus L.) sounds

Female and juvenile haddock make sounds, as well as males. Examination of the sounds from different sexes indicates that the sound waveform is a function of fish maturity and it is gender-specific. Immature fish sounds were found to be made up of two pulses with similar frequencies and opposite polarities. Females produced two pulses with the same polarity, the first pulse having a higher frequency than the second. The acoustic characteristics of juvenile, female and male haddock sounds are compared. Sexual dimorphism in the mass of the drumming muscle mass has also been investigated. Female haddock possess less well-developed drumming muscles than males throughout the whole year. A significant difference in drumming muscle mass was observed not only in males but also in females at different seasons. A positive relation between drumming muscle mass and fish size has been highlighted in both male and female fish. The physical parameters of the sound units emitted by juveniles, females and males, which are likely affected by physiological condition and maturity stage, are discussed in relation to the sound-producing mechanism.