Behavioural response to boat noise weakens the strength of a trophic link in coral reefs.

In oceans, the noise generated by human activities has reached phenomenal proportions, with considerable harmful effects on marine life. Measuring this impact to achieve a sustainable balance for highly vulnerable marine ecosystems, such as coral reefs, is a critical environmental policy objective. Here, we demonstrate that anthropogenic noise alters the interactions of a coral reef fish with its environment and how this behavioural response to noise impairs foraging. In situ observations on the Moorea reef revealed that the damselfish Dascyllus emamo reacts to boat passage by moving closer to its coral bommie, considerably reducing the volume of water available to search for prey. Using boat noise playback experiments in microcosms, we studied D. emamo's behaviour and modeled its functional response (FR), which is the relationship between resource use and resource density, when feeding on juvenile shrimps. Similar to field observations, noise reduced D. emamo's spatial occupancy, accompanied by a lower FR, indicating a reduction in predation independent of prey density. Overall, noise-induced behavioural changes are likely to influence predator-prey interaction dynamics and ultimately the fitness of both protagonists. While there is an urgent need to assess the effect of anthropogenic noise on coral reefs, the ecological framework of the FR approach combined with behavioural metrics provides an essential tool for evaluating the cascading effects of noise on nested ecological interactions at the community level.

Coral reef fish density at a tourist destination responded rapidly to COVID-19 restrictions.

Throughout the world, anthropogenic pressure on natural ecosystems is intensifying, notably through urbanisation, economic development, and tourism. Coral reefs have become exposed to stressors related to tourism. To reveal the impact of human activities on fish communities, we used COVID-19-related social restrictions in 2021. In French Polynesia, from February to December 2021, there was a series of restrictions on local activities and international tourism. We assessed the response of fish populations in terms of changes in the species richness and density of fish in the lagoon of Bora-Bora (French Polynesia). We selected sites with varying human pressures-some dedicated to tourism activities, others affected by boat traffic, and control sites with little human presence. Underwater visual surveys demonstrated that fish density and richness differed spatially and temporally. They were lowest on sites affected by boat traffic regardless of pandemic-related restrictions, and when activities were authorised; they were highest during lockdowns. Adult fish density increased threefold on sites usually affected by boat traffic during lockdowns and increased 2.7-fold on eco-tourism sites during international travel bans. Human activities are major drivers of fish density and species richness spatially across the lagoon of Bora-Bora but also temporally across pandemic-related restrictions, with dynamic responses to different restrictions. These results highlight the opportunity provided by pauses in human activities to assess their impact on the environment and confirm the need for sustainable lagoon management in Bora-Bora and similar coral reef settings affected by tourism and boat traffic.

Invertebrate sounds from photic to mesophotic coral reefs reveal vertical stratification and diel diversity.

Although mesophotic coral ecosystems account for approximately 80% of coral reefs, they remain largely unexplored due to their challenging accessibility. The acoustic richness within reefs has led scientists to consider passive acoustic monitoring as a reliable method for studying both altiphotic and mesophotic coral reefs. We investigated the relationship between benthic invertebrate sounds (1.5-22.5 kHz), depth, and benthic cover composition, key ecological factors that determine differences between altiphotic and mesophotic reefs. Diel patterns of snaps and peak frequencies were also explored at different depths to assess variations in biorhythms. Acoustic recorders were deployed at 20 m, 60 m, and 120 m depths across six islands in French Polynesia. The results indicated that depth is the primary driver of differences in broadband transient sound (BTS) soundscapes, with sound intensity decreasing as depth increases. At 20-60 m, sounds were louder at night. At 120 m depth, benthic activity rhythms exhibited low or highly variable levels of diel variation, likely a consequence of reduced solar irradiation. On three islands, a peculiar peak in the number of BTS was observed every day between 7 and 9 PM at 120 m, suggesting the presence of cyclic activities of a specific species. Our results support the existence of different invertebrate communities or distinct behaviors, particularly in deep mesophotic reefs. Overall, this study adds to the growing evidence supporting the use of passive acoustic monitoring to describe and understand ecological patterns in mesophotic reefs.

Production of sounds by squirrelfish during symbiotic relationships with cleaner wrasses.

Examples of symbiotic relationships often include cleaning mutualisms, typically involving interactions between cleaner fish and other fish, called the clients. While these cleaners can cooperate by removing ectoparasites from their clients, they can also deceive by feeding on client mucus, a behavior usually referred to as "cheating behavior" that often leads to a discernible jolt from the client fish. Despite extensive studies of these interactions, most research has focused on the visual aspects of the communication. In this study, we aimed to explore the role of acoustic communication in the mutualistic relationship between cleaner fishes and nine holocentrid client species across four regions of the Indo-Pacific Ocean: French Polynesia, Guam, Seychelles, and the Philippines. Video cameras coupled with hydrophones were positioned at various locations on reefs housing Holocentridae fish to observe their acoustic behaviors during interactions. Our results indicate that all nine species of holocentrids can use acoustic signals to communicate to cleaner fish their refusal of the symbiotic interaction or their desire to terminate the cooperation. These sounds were predominantly observed during agonistic behavior and seem to support visual cues from the client. This study provides a novel example of acoustic communication during a symbiotic relationship in teleosts. Interestingly, these vocalizations often lacked a distinct pattern or structure. This contrasts with numerous other interspecific communication systems where clear and distinguishable signals are essential. This absence of a clear acoustic pattern may be because they are used in interspecific interactions to support visual behavior with no selective pressure for developing specific calls required in conspecific recognition. The different sound types produced could also be correlated with the severity of the client response. There is a need for further research into the effects of acoustic behaviors on the quality and dynamics of these mutualistic interactions.

Diving into dual functionality: Swim bladder muscles in lionfish for buoyancy and sonic capabilities.

Although the primary function of the swim bladder is buoyancy, it is also involved in hearing, and it can be associated with sonic muscles for voluntary sound production. The use of the swim bladder and associated muscles in sound production could be an exaptation since this is not its first function. We however lack models showing that the same muscles can be used in both movement and sound production. In this study, we investigate the functions of the muscles associated with the swim bladder in different Pteroinae (lionfish) species. Our results indicate that Pterois volitans, P. radiata and Dendrochirus zebra are able to produce long low-frequency hums when disturbed. The deliberate movements of the fin spines during sound production suggest that these sounds may serve as aposematic signals. In P. volitans and P. radiata, hums can be punctuated by intermittent louder pulses called knocks. Analysis of sonic features, morphology, electromyography and histology strongly suggest that these sounds are most likely produced by muscles closely associated with the swim bladder. These muscles originate from the neurocranium and insert on the posterior part of the swim bladder. Additionally, cineradiography supports the hypothesis that these same muscles are involved in altering the swim bladder's length and angle, thereby influencing the pitch of the fish body and participating in manoeuvring and locomotion movements. Fast contraction of the muscle should be related to sound production whereas sustained contractions allows modifications in swim bladder shape and body pitch.

Reliable characterization of sound features in fishes begins in open-water environmentsa).

Many fishes use sounds to communicate in a wide range of behavioral contexts. In monitoring studies, these sounds can be used to detect and identify species. However, being able to confidently link a sound to the correct emitting species requires precise acoustical characterization of the signals in controlled conditions. For practical reasons, this characterization is often performed in small sized aquaria, which, however, may cause sound distortion, and prevents an accurate description of sound characteristics that will ultimately impede sound-based species identification in open-water environments. This study compared the sounds features of five specimens of the silverspot squirrelfish Sargocentron caudimaculatum recorded at sea and in aquaria of different sizes and materials. Our results point out that it is preferable to record fish sounds in an open-water environment rather than in small aquaria because acoustical features are affected (sound duration and dominant frequency) when sounds are recorded in closed environments as a result of reverberation and resonance. If not possible, it is recommended that (1) sound recordings be made in plastic or plexiglass aquaria with respect to glass aquaria and (2) aquaria with the largest dimensions and volumes be chosen.

The multi-level regulation of clownfish metamorphosis by thyroid hormones.

Most marine organisms have a biphasic life cycle during which pelagic larvae transform into radically different juveniles. In vertebrates, the role of thyroid hormones (THs) in triggering this transition is well known, but how the morphological and physiological changes are integrated in a coherent way with the ecological transition remains poorly explored. To gain insight into this question, we performed an integrated analysis of metamorphosis of a marine teleost, the false clownfish (Amphiprion ocellaris). We show how THs coordinate a change in color vision as well as a major metabolic shift in energy production, highlighting how it orchestrates this transformation. By manipulating the activity of liver X regulator (LXR), a major regulator of metabolism, we also identify a tight link between metabolic changes and metamorphosis progression. Strikingly, we observed that these regulations are at play in the wild, explaining how hormones coordinate energy needs with available resources during the life cycle.

'Habitat-associated soundscape' hypothesis tested on several coral reefs within a lagoon (Bora-Bora Island, French Polynesia).

Coral reefs encompass different habitats that have their own living communities. The present study aimed to test the hypothesis that these different kinds of habitats were characterized by specific soundscapes. Within the lagoon of Bora-Bora, acoustic recordings and visual surveys of substrate type and fish communities were conducted on four reef sites belonging to the three main geomorphological habitats (fringing reef, channel reef, barrier reef) from February to April 2021. Two acoustic parameters were measured for each site and month, during the day and at night: the peak frequency (Fpeak, in Hz) and the corresponding power spectral density (PSDpeak, in dB re 1 µPa2 Hz-1). Our results showed that each geomorphological unit could be characterized by these two parameters and therefore had a specific acoustic signature. Moreover, our study showed that a higher living coral cover was significantly positively correlated with Fpeak in the low-frequency band (50-2000 Hz) during day-time. Although biodiversity indices based on visual surveys did not differ significantly, fish communities and soundscapes were significantly different between sites. Overall, our study underlines the importance of passive acoustics in coral reef monitoring as soundscapes are habitat specific. Supplementary Information: The online version contains supplementary material available at 10.1007/s00227-023-04206-3.

Roadside sales activities in a South Pacific Island (Bora-Bora) reveal sustainable strategies for local food supply during a pandemic.

During the COVID-19 pandemic, the reduced exports and imports as well as the lack of activity due to the interruption in the international tourism economy seriously impacted food security in many Pacific Islands. People often returned to natural resources to provide for themselves, their families, or to generate income. On Bora-Bora Island, the major tourist destination in French Polynesia, roadside sales are widespread. Our study analyses the impact of the COVID-19 pandemic on roadside sales activities through a census of roadside stalls on the five Bora-Bora districts conducted before (January and February 2020), during (from March 2020 to October 2021) and after (from November to December 2021) health-related activity and travel restrictions. Our results showed that the marketing system for local products (fruits, vegetables, cooked meals, and fish) increased in the form of roadside sales during the COVID-19 in two of the five districts of Bora-Bora. Roadside selling would be an alternative system for providing food to the population at Bora-Bora during a global crisis and that could reveal itself sustainable after this pandemic.

Differences in the behavior and diet between shoaling and solitary surgeonfish (Acanthurus triostegus).

Variation in behavior within marine and terrestrial species can influence the functioning of the ecosystems they inhabit. However, the contribution of social behavior to ecosystem function remains underexplored. Many coral reef fish species provide potentially insightful models for exploring how social behavior shapes ecological function because they exhibit radical intraspecific variation in sociality within a shared habitat. Here, we provide an empirical exploration on how the ecological function of a shoaling surgeonfish (Acanthurus triostegus) may differ from that of solitary conspecifics on two Pacific coral reefs combining insight from behavioral observations, stable isotope analysis, and macronutrient analysis of gut and fecal matter. We detected important differences in how the social mode of A. triostegus affected its spatial and feeding ecology, as well as that of other reef fish species. Specifically, we found increased distance traveled and area covered by shoaling fish relative to solitary A. triostegus. Additionally, shoaling A. triostegus primarily grazed within territories of other herbivorous fish and had piscivorous and nonpiscivorous heterospecific fish associated with the shoal, while solitary A. triostegus grazed largely grazed outside of any territories and did not have any such interactions with heterospecific fish. Results from stable isotope analysis show a difference in δ15N isotopes between shoaling and solitary fish, which suggests that these different social modes are persistent. Further, we found a strong interaction between social behavior and site and carbohydrate and protein percentages in the macronutrient analysis, indicating that these differences in sociality are associated with measurable differences in both the feeding ecology and nutrient excretion patterns. Our study suggests that the social behavior of individuals may play an important and underappreciated role in mediating their ecological function.

Targeted census of lionfishes (Scorpaenidae) reveals high densities in their native range.

Indo-Pacific lionfishes generally exhibit cryptic behaviours and so can be missed when conducting non-targeted surveys. Here, the authors report the results from targeted surveys of lionfish at Moorea, French Polynesia. Lionfish from three species (Pterois antennata, Pterois radiata, Dendrochirus biocellatus) were observed at a mean density of 267 individuals ha-1 . This is substantially higher than previous estimates from the same area (Moorea) and represents the highest reported density of lionfishes from their Pacific range. Overall, this study highlights the importance of targeted survey techniques for detecting cryptic species on coral reefs.

Developing and adult reef fish show rapid light-induced plasticity in their visual system.

The visual capabilities of fish are optimized for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e.g., ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short-term changes in the light environment, e.g., algal blooms and light pollution. In this study, we investigated the effect of short-term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in juvenile and adult diurnal reef fish (convict surgeonfish; Acanthurus triostegus). Results revealed phenotypic plasticity in the retina across ontogeny, particularly during development. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light and simulated artificial light at night had a lesser effect. Under dim light, juveniles and adults increased absolute expression of the cone opsin genes, sws2a, rh2c and lws, within a few days and juveniles also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes potentially enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species' natural light environment, i.e., a diurnal fish in "constant night". Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 h. Overall, our study showed rapid, reversible light-induced changes in the retina of A. triostegus, demonstrating phenotypic plasticity in the visual system of a reef fish throughout life.

Effects of COVID-19 lockdown on the observed density of coral reef fish along coastal habitats of Moorea, French Polynesia.

During the first COVID-19 lockdown in 2020, levels of coastal activities such as subsistence fishing and marine tourism declined rapidly throughout French Polynesia. Here, we examined whether the reduction in coastal use led to changes in fish density around the island of Moorea. Two natural coastal marine habitats (bare sand and mangrove) and one type of man-made coastal structure (embankment) were monitored on the west coast of the island before and after the first COVID-19 lockdown. At the end of the lockdown (May 2020), significantly higher apparent densities of juvenile and adult fish, including many harvested species, were recorded compared to levels documented in 2019 at the same period (April 2019). Fish densities subsequently declined as coastal activities recovered; however, 2 months after the end of the lockdown (July 2020), densities were still higher than they were in July 2019 with significant family-specific variation across habitats. This study highlights that short-term reductions in human activity can have a positive impact on coastal fish communities and may encourage future management policy that minimizes human impacts on coastline habitats. Supplementary Information: The online version contains supplementary material available at 10.1007/s10113-022-02011-0.

COVID-19 lockdown highlights impact of recreational activities on the behaviour of coral reef fishes.

In 2020, the COVID-19 pandemic led to a reduction in human activities and restriction of all but essential movement for much of the world's population. A large, but temporary, increase in air and water quality followed, and there have been several reports of animal populations moving into new areas. Extending on long-term monitoring efforts, we examined how coral reef fish populations were affected by the government-mandated lockdown across a series of Marine Protected Area (MPA) and non-Marine Protected Area (nMPA) sites around Moorea, French Polynesia. During the first six-week lockdown that Moorea experienced between March and May 2020, increases (approx. two-fold) in both harvested and non-harvested fishes were observed across the MPA and nMPA inner barrier reef sites, while no differences were observed across the outer barrier sites. Interviews with local amateur and professional fishers indicated that while rules regarding MPA boundaries were generally followed, some subsistence fishing continued in spite of the lockdown, including within MPAs. As most recreational activities occur along the inner reef, our data suggest that the lockdown-induced reduction in recreational activities resulted in the recolonization of these areas by fishes, highlighting how fish behaviour and space use can rapidly change in our absence.

Development of dim-light vision in the nocturnal reef fish family Holocentridae. II: Retinal morphology.

Ontogenetic changes in the habitats and lifestyles of animals are often reflected in their visual systems. Coral reef fishes start life in the shallow open ocean but inhabit the reef as juveniles and adults. Alongside this change in habitat, some species also change lifestyles and become nocturnal. However, it is not fully understood how the visual systems of nocturnal reef fishes develop and adapt to these significant ecological shifts over their lives. Therefore, we used a histological approach to examine visual development in the nocturnal coral reef fish family, Holocentridae. We examined 7 representative species spanning both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes). Pre-settlement larvae showed strong adaptation for photopic vision with high cone densities and had also started to develop a multibank retina (i.e. multiple rod layers), with up to two rod banks present. At reef settlement, holocentrids showed greater adaptation for scotopic vision, with higher rod densities and higher summation of rods onto the ganglion cell layer. By adulthood, they had well-developed scotopic vision with a highly rod-dominated multibank retina comprising 5-17 rod banks and enhanced summation of rods onto the ganglion cell layer. Although the ecological demands of the two subfamilies were similar throughout their lives, their visual systems differed after settlement, with Myripristinae showing more pronounced adaptation for scotopic vision than Holocentrinae. Thus, it is likely that both ecology and phylogeny contribute to the development of the holocentrid visual system.

Development of dim-light vision in the nocturnal reef fish family Holocentridae. I: Retinal gene expression.

Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well adapted to photopic conditions with pre-settlement larvae having high levels of cone opsin gene expression and a broad cone opsin gene repertoire (8 genes). At reef settlement, holocentrids started to invest more in their scotopic visual system, and compared with adults, showed upregulation of genes involved in cell differentiation/proliferation. By adulthood, holocentrids had well developed scotopic vision with high levels of rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems diverged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny are likely to determine the development of the holocentrid visual system.

Harbours as unique environmental sites of multiple anthropogenic stressors on fish hormonal systems.

Fish development and acclimation to environmental conditions are strongly mediated by the hormonal endocrine system. In environments contaminated by anthropogenic stressors, hormonal pathway alterations can be detrimental for growth, survival, fitness, and at a larger scale for population maintenance. In the context of increasingly contaminated marine environments worldwide, numerous laboratory studies have confirmed the effect of one or a combination of pollutants on fish hormonal systems. However, this has not been confirmed in situ. In this review, we explore the body of knowledge related to the influence of anthropogenic stressors disrupting fish endocrine systems, recent advances (focusing on thyroid hormones and stress hormones such as cortisol), and potential research perspectives. Through this review, we highlight how harbours can be used as "in situ laboratories" given the variety of anthropogenic stressors (such as plastic, chemical, sound, light pollution, and invasive species) that can be simultaneously investigated in harbours over long periods of time.

Plicidentine in the oral fangs of parrotfish (Scarinae, Labriformes).

Parrotfish play important ecological roles in coral reef and seagrass communities across the globe. Their dentition is a fascinating object of study from an anatomical, functional and evolutionary point of view. Several species maintained non-interlocked dentition and browse on fleshy algae, while others evolved a characteristic beak-like structure made of a mass of coalesced teeth that they use to scrape or excavate food off hard limestone substrates. While parrotfish use their highly specialized marginal teeth to procure their food, they can also develop a series of large fangs that protrude from the upper jaw, and more rarely from the lower jaw. These peculiar fangs do not participate in the marginal dentition and their function remains unclear. Here we describe the morphology of these fangs and their developmental relationship to the rest of the oral dentition in the marbled parrotfish (Leptoscarus vaigiensis), the star-eye parrotfish (Calotomus carolinus), and the palenose parrotfish (Scarus psittacus). Through microtomographic and histological analyses, we show that some of these fangs display loosely folded plicidentine along their bases, a feature that has never been reported in parrotfish. Plicidentine is absent from the marginal teeth and is therefore exclusive to the fangs. Parrotfish fangs develop a particular type of simplexodont plicidentine with a pulpal infilling of alveolar bone at later stages of dental ontogeny. The occurrence of plicidentine and evidence of extensive tooth wear, and even breakage, lead us to conclude that the fangs undergo frequent mechanical stress, despite not being used to acquire food. This strong mechanical stress undergone by fangs could be linked either to forced contact with congeners or with the limestone substrate during feeding. Finally, we hypothesize that the presence of plicidentine in parrotfish is not derived from a labrid ancestor, but is probably a recently evolved trait in some parrotfish taxa, which may even have evolved convergently within this subfamily.