Loïc Kéver

Environmental constraints drive the partitioning of the soundscape in fishes

Significance More and more studies stress the potential deleterious effect of anthropogenic sounds on fish acoustic communication. Paradoxically, how the communication between fishes in a community is organized remains extremely poorly known, as studies using passive acoustic recordings are typically restricted to one or two species. At a single site, we were able to follow 16 different vertebrate sounds for 15 days. We demonstrate that the fish population can be distributed into two groups: one diurnal and one nocturnal. Most interestingly, fish calling at night do not show overlap at the level of the main calling frequency, in contrast to fish calling during the day. This shows that at night, in the absence of visual cues, sound communication is more important. The underwater environment is more and more being depicted as particularly noisy, and the inventory of calling fishes is continuously increasing. However, it currently remains unknown how species share the soundscape and are able to communicate without misinterpreting the messages. Different mechanisms of interference avoidance have been documented in birds, mammals, and frogs, but little is known about interference avoidance in fishes. How fish thus partition the soundscape underwater remains unknown, as acoustic communication and its organization have never been studied at the level of fish communities. In this study, passive acoustic recordings were used to inventory sounds produced in a fish community (120 m depth) in an attempt to understand how different species partition the acoustic environment. We uncovered an important diversity of fish sounds, and 16 of the 37 different sounds recorded were sufficiently abundant to use in a quantitative analysis. We show that sonic activity allows a clear distinction between a diurnal and a nocturnal group of fishes. Moreover, frequencies of signals made during the day overlap, whereas there is a clear distinction between the different representatives of the nocturnal callers because of a lack of overlap in sound frequency. This first demonstration, to our knowledge, of interference avoidance in a fish community can be understood by the way sounds are used. In diurnal species, sounds are mostly used to support visual display, whereas nocturnal species are generally deprived of visual cues, resulting in acoustic constraints being more important.

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.

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.

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.

Sound production in Onuxodon fowleri (Carapidae) and its amplification by the host shell

Onuxodon species are well known for living inside pearl oysters. As in other carapids, their anatomy highlights their ability to make sounds but sound production has never been documented in Onuxodon. This paper describes sound production in Onuxodon fowleri as well as the anatomy of the sound production apparatus. Single-pulsed sounds and multiple-pulsed sounds that sometimes last more than 3 s were recorded in the field and in captivity (Makemo Island, French Polynesia). These pulses are characterized by a broadband frequency spectrum from 100 to 1000 Hz. Onuxodon fowleri is mainly characterized by its ability to modulate the pulse period, meaning that this species can produce pulsed sounds and tonal-like sounds using the same mechanism. In addition, the sound can be remarkably amplified by the shell cavity (peak gain can exceed 10 dB for some frequencies). The sonic apparatus of O. fowleri is characterized by a rocker bone in front of the swimbladder, modified vertebrae and epineurals, and two pairs of sonic muscles, one of which (primary sonic muscle) inserts on the rocker bone. The latter structure, which is absent in other carapid genera, appears to be sexually dimorphic suggesting differences in sound production in males and females. Sound production in O. fowleri could be an example of adaptation where an animal exploits features of its environment to enhance communication.

Hearing capacities and otolith size in two ophidiiform species (Ophidion rochei and Carapus acus)

Numerous studies have highlighted the diversity of fish inner ear morphology. However, the function of the shape, size and orientation of the different structures remains poorly understood. The saccule (otolithic endorgan) is considered to be the principal hearing organ in fishes and it has been hypothesized that sagitta (saccular otolith) shape and size affect hearing capacities: large sagittae are thought to increase sensitivity. The sagittae of many ophidiids and carapids occupy a large volume inside the neurocranium. Hence they are a good structure with which to test the size hypothesis. The main aim of this study was to investigate hearing capacities and inner ear morphology in two ophidiiform species: Ophidion rochei and Carapus acus. We used a multidisciplinary approach that combines dissections, μCT-scan examinations and auditory evoked potential techniques. Carapus acus and O. rochei sagittae have similar maximal diameters; both species have larger otoliths than many non-ophidiiform species, especially compared with the intra-neurocranium volume. Both species are sensitive to sounds up to 2100 Hz. Relative to the skull, O. rochei has smaller sagittae than the carapid, but better hearing capacities from 300 to 900 Hz and similar sensitivities at 150 Hz and from 1200 to 2100 Hz. Results show that hearing capacities of a fish species cannot be predicted only based on sagitta size. Larger otoliths (in size relative to the skull) may have evolved mainly for performing vestibular functions in fishes, especially those species that need to execute precise and complex movements.

Effects of seawater temperature on sound characteristics in Ophidion rochei (Ophidiidae)

Although the sound production mechanisms of male and female Ophidion rochei (Ophidiidae) differ significantly, temperature affects them in the same manner. In both sexes, temperature correlated negatively with pulse period and positively with sound frequencies but had no, or weak effects on other sound characteristics.

Neurogenomic profiling reveals distinct gene expression profiles between brain parts that are consistent in ophthalmotilapia cichlids

The detection of external and internal cues alters gene expression in the brain which in turn may affect neural networks that underly behavioral responses. Previous studies have shown that gene expression profiles differ between major brain regions within individuals and between species with different morphologies, cognitive abilities and/or behaviors. A detailed description of gene expression in all macroanatomical brain regions and in species with similar morphologies and behaviors is however lacking. Here, we dissected the brain of two cichlid species into six macroanatomical regions. Ophthalmotilapia nasuta and O. ventralis have similar morphology and behavior and occasionally hybridize in the wild. We use 3′ mRNA sequencing and a stage-wise statistical testing procedure to identify differential gene expression between females that were kept in a social setting with other females. Our results show that gene expression differs substantially between all six brain parts within species: out of 11,577 assessed genes, 8,748 are differentially expressed (DE) in at least one brain part compared to the average expression of the other brain parts. At most 16% of these DE genes have |log2FC| significantly higher than two. Functional differences between brain parts were consistent between species. The majority (61–79%) of genes that are DE in a particular brain part were shared between both species. Only 32 genes show significant differences in fold change across brain parts between species. These genes are mainly linked to transport, transmembrane transport, transcription (and its regulation) and signal transduction. Moreover, statistical equivalence testing reveals that within each comparison, on average 89% of the genes show an equivalent fold change between both species. The pronounced differences in gene expression between brain parts and the conserved patterns between closely related species with similar morphologies and behavior suggest that unraveling the interactions between genes and behavior will benefit from neurogenomic profiling of distinct brain regions.

Correction: Unusual sound production mechanism in the triggerfish Rhinecanthus aculeatus (Balistidae)

There was an error published in J. Exp. Biol. 220 , [186-193][1]. The surname of Sam Van Wassenbergh was incorrectly displayed. This has been corrected in the online full-text and PDF versions. The authors apologise for any inconvenience this may have caused. [1]: /lookup/volpage/220/186?iss=2