Ontogenesis of agonistic vocalizations in the cichlid fish Metriaclima zebra

While acoustic communication has been described in adults of various fish species, our knowledge about the ontogeny of fish sound production is limited. In adults, sound signals are known to be involved during aggressive interactions. However, aggressive behaviour may appear early in the life of fishes due to the possible competition for food and space. If acoustic signals are used to send information to competitors, sounds are likely to play a role during interactions between juvenile fish as well. The apparition and evolution of sound production were monitored in a group of juveniles of the cichlid fish Metriaclima zebra from hatching to 4months of age. In addition, the link between vocalizations and agonistic behaviour was studied during dyadic interactions at three different ages. Sounds production appeared to be present early in the development of this fish and increased along with the number of aggressive behaviours. Recorded sounds consisted, in juveniles, in isolated pulses showing a decrease in frequency and duration as the fish grew. In adults, sounds became bursts of pulses but the transition from isolated to repetitive pulses was not observed. These results are compared to the existing literature on sound production ontogeny in fishes.     

Innate sound production in the cichlid Oreochromis niloticus

The mouthbrooding cichlid Oreochromis niloticus is one of the world's best-studied fish and is raised extensively for aquaculture. Although it is a common behavioural model, its acoustic communication has been neglected. Because of extensive parental care, the species is a good candidate for vocal learning. In male O. niloticus , we investigated for the first time sound production in agonistic interactions during nest construction. Males produce short-duration (250–400 ms), often double-pulse sounds. Most energy is below 200 Hz and includes three main low-frequency peaks although energy extends beyond 1 kHz. Males (separated as eggs and raised in isolation) produce similar sounds in the same context as parental fish, indicating that the ability to produce sounds and the basic properties of the sounds are innate.     

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.     

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.     

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.     

Contribution to the study of acoustic communication in two Belgian river bullheads (<Emphasis Type="Italic">Cottus rhenanus and C. perifretum</Emphasis>) with further insight into the sound-producing mechanism

Background

The freshwater sculpins (genus Cottus) are small, bottom-living fishes widely distributed in North America and Europe. The taxonomy of European species has remained unresolved for a long time due to the overlap of morphological characters. Sound production has already been documented in some cottid representatives, with sounds being involved in courtship and agonistic interactions. Although the movements associated with sound production have been observed, the underlying mechanism remains incomplete. Here, we focus on two closely related species from Belgium: C. rhenanus and C. perifretum. This study aims 1) to record and to compare acoustic communication in both species, 2) to give further insight into the sound-producing mechanism and 3) to look for new morphological traits allowing species differentiation.

Results

Both Cottus species produce multiple-pulsed agonistic sounds using a similar acoustic pattern: the first interpulse duration is always longer, making the first pulse unit distinct from the others. Recording sound production and hearing abilities showed a clear relationship between the sound spectra and auditory thresholds in both species: the peak frequencies of calls are around 150 Hz, which corresponds to their best hearing sensitivity. However, it appears that these fishes could not hear acoustic signals produced by conspecifics in their noisy habitat considering their hearing threshold expressed as sound pressure (~ 125 dB re 1 μPa). High-speed video recordings highlighted that each sound is produced during a complete back and forth movement of the pectoral girdle.

Conclusions

Both Cottus species use an acoustic pattern that remained conserved during species diversification. Surprisingly, calls do not seem to have a communicative function. On the other hand, fish could detect substrate vibrations resulting from movements carried out during sound production. Similarities in temporal and spectral characteristics also suggest that both species share a common sound-producing mechanism, likely based on pectoral girdle vibrations. From a morphological point of view, only the shape of the spinelike scales covering the body allows species differentiation.

     

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.     

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 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].     

Acoustic threat displays and agonistic behaviour in the red-finned loach <Emphasis Type="Italic">Yasuhikotakia modesta</Emphasis>

Agonistic behaviour and the significance of acoustic threat displays were investigated in juvenile red-finned loaches, Yasuhikotakia modesta. This species produced two different vocalizations during agonistic encounters—clicks and butting sounds. Clicks were produced at some distance from the opponent whereas butting sounds were emitted when one fish touched the other with its mouth. This occurred primarily during circling. Both sound types were short broadband signals with the main energies concentrated at about 230 Hz, but clicks were longer in duration and lower in sound level. Agonistic behaviour usually started when one fish approached the other, spread its fins and produced clicks (threat displays), which was followed by parallel displaying, circling and chasing. All fish approached a mirror quickly and displayed aggressively in a parallel position. The number and duration of the threat displays in front of the mirror image were significantly elevated compared with control experiments (rear of the mirror). When playing back click trains in the presence of a mirror image, loaches vocalized significantly less often than during the silent periods, whereas the amount of lateral displaying remained similar. These data indicate that agonistic sounds reduced acoustic displays in red-finned loaches.     

Brood-directed parental aggression and early brood loss in the coral reef fish, Acanthochromis polyacanthus (Pomacentridae)

Brood-directed parental aggression, in which parents attack and even kill their own young, is described for the coral reef fish Acanthochromis polyacanthus. This behaviour involves both parents, occurs on days 7–16 post-hatching, and is characteristic of all broods produced early in the spawning season. Such parental aggression appears to underlie widespread early brood loss in the species, i.e. disappearance of young before they reach an age at which they are viable in the absence of parental defence. Simultaneously, there is also a high frequency of sudden increases in the sizes of some tended broods. The data suggest that some brood-tending parents are forcibly expelling their broods from parental territories, and fostering them on to adults still tending broods. By expelling their young and re-spawning, pairs may realize a 7% increase in annual fecundity over pairs that do not expel their young, despite a low survival rate of expelled young.     

Fish Sound Production in the Presence of Harmful Algal Blooms in the Eastern Gulf of Mexico

This paper presents the first known research to examine sound production by fishes during harmful algal blooms (HABs). Most fish sound production is species-specific and repetitive, enabling passive acoustic monitoring to identify the distribution and behavior of soniferous species. Autonomous gliders that collect passive acoustic data and environmental data concurrently can be used to establish the oceanographic conditions surrounding sound-producing organisms. Three passive acoustic glider missions were conducted off west-central Florida in October 2011, and September and October 2012. The deployment period for two missions was dictated by the presence of red tide events with the glider path specifically set to encounter toxic Karenia brevis blooms (a.k.a red tides). Oceanographic conditions measured by the glider were significantly correlated to the variation in sounds from six known or suspected species of fish across the three missions with depth consistently being the most significant factor. At the time and space scales of this study, there was no detectable effect of red tide on sound production. Sounds were still recorded within red tide-affected waters from species with overlapping depth ranges. These results suggest that the fishes studied here did not alter their sound production nor migrate out of red tide-affected areas. Although these results are preliminary because of the limited measurements, the data and methods presented here provide a proof of principle and could serve as protocol for future studies on the effects of algal blooms on the behavior of soniferous fishes. To fully capture the effects of episodic events, we suggest that stationary or vertically profiling acoustic recorders and environmental sampling be used as a complement to glider measurements.     

The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2-5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.     

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.     

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.     

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.     

Spawning vocalizations in male freshwater gobiids (Pisces,Gobiidae)

Synopsis Males of two freshwater Italian gobies, the common goby, Padogobius martensii and the panzarolo goby, Knipowitschia punctatissima, emit trains of low-frequency pulses, i.e. drumming sounds, in the presence of a ripe female in the nest. In P, martensii the drumming sound is usually followed by a tonal sound (complex sound). Examination of the pulse structure suggests that these sounds are produced by muscles acting on the swimbladder. Both species exhibited high emission rates of spawning sounds, especially before the beginning of oviposition. Moreover, spawning sound production ceased only after the female abandoned the nest, which always occurred at the end of oviposition. This is the first study reporting the production among fishes of distinct sounds during protracted spawning. Unlike sounds produced just before mating by fishes with planktonic or demersal zygotes, the spawning sound production of these gobies does not function to coordinate mating events in the nest. The presence of a two-part vocalization by male P. martensii even suggests a functional dichotomy of spawning sounds in this species.     

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.