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.

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.

'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.

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.

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.

Effects of COVID-19 pandemic restrictions on coral reef fishes at eco-tourism sites in Bora-Bora, French Polynesia.

The COVID-19 pandemic led to a global lockdown in mid-2020, leading to a rapid decline in international travel and tourism. In French Polynesia, marine-based tourism activities ceased in March 2020 with the suspension of international flights (i.e., 45 days - between 20th March and 04th May 2020), slowly restarting between May-July as domestic and international visitors returned. The impacts of this rapid change in human activity at reef tourism sites on associated reef fishes was examined at Bora-Bora Island through underwater surveys of five control and nine eco-tourism sites. Our results showed that fish density significantly increased from March to May (i.e., the overall density of fishes increased by 143% and harvested species by 215%), but returned to pre-lockdown levels by August 2020. At the usually busy eco-tourism sites, fish diversity, notably of piscivores, omnivores, and benthic feeders, was higher in the absence of tourists. The impact observed is almost certainly related to short term changes in fish behavior, as any density fluctuations at the population level are unlikely to have happened over such a short time frame. Overall, these findings highlight the influence of human activities on fish communities and underline the need for further research to evaluate the environmental impacts of eco-tourism.

Changes to an urban marina soundscape associated with COVID-19 lockdown in Guadeloupe.

In 2020, the COVID-19 pandemic led to government-enforced limits on activities worldwide, causing a marked reduction of human presence in outdoors environments, including in coastal areas that normally support substantial levels of boat traffic. These restrictions provided a unique opportunity to quantify the degree to which anthropogenic noise contributes to and impacts underwater soundscapes. In Guadeloupe, French West Indies, a significantly lower number of motor boats were recorded in the vicinity of the major urban marina during the peak of the first COVID-19 lockdown (April-May 2020), compared with the number recorded post-lockdown. The resumption of human activities at the end of May was correlated with a maximum increase of 6 decibels in the ambient noise level underwater. The change in noise level did not impact daily sound production patterns of vocal fishes, with increased activity at dusk seen both during and after the lockdown period. However, during the lockdown vocal activity was comprised of a reduced number of sounds, suggesting that anthropogenic noise has the potential to interfere with vocalization behaviours in fishes.

Long term relationship between farming damselfish, predators, competitors and benthic habitat on coral reefs of Moorea Island.

Understanding the processes that shape biodiversity is essential for effective environmental management. Across the world's coral reefs, algal farming damselfish (Stegastes sp.) modify the surrounding benthic community through their creation of algae "farms". Using a long-term monitoring dataset (2005-2019) from Moorea Island, French Polynesia, we investigated whether the density of dusky damselfish (Stegastes nigricans) is associated with benthic habitat composition, the density of predators and/or competitors, and whether the survey area was inside or outside of a Marine Protected Area (MPA). We found no evidence that benthic cover or number of competitors were associated with dusky damselfish densities, both inside and outside MPAs. In contrast, fluctuations in dusky damselfish densities were negatively associated with the density of predators (e.g. Serranidae, Muraenidae and Scorpaenidae) in the preceding year in non-MPA areas, and both within and outside of MPAs when predator densities were high (2005-2010). These results suggest that healthy predator populations may be important for regulating the abundances of keystone species, such as algal farming damselfish, especially when predator densities are high.

Noise pollution on coral reefs? - A yet underestimated threat to coral reef communities.

Noise pollution is an anthropogenic stressor that is increasingly recognized for its negative impact on the physiology, behavior and fitness of marine organisms. Driven by the recent expansion of maritime shipping, artisanal fishing and tourism (e.g., motorboats used for recreational purpose), underwater noise increased greatly on coral reefs. In this review, we first provide an overview on how reef organisms sense and use sound. Thereafter we review the current knowledge on how underwater noise affects different reef organisms. Although the majority of available examples are limited to few fish species, we emphasize how the impact of noise differs based on an organisms' acoustic sensitivity, mobility and developmental stage, as well as between noise type, source and duration. Finally, we highlight measures available to governments, the shipping industry and individual users and provide directions for polices and research aimed to manage this global issue of noise emission on coral reefs.

The development of hearing abilities in the shark Scyliorhinus canicula.

The few works on audition in sharks and rays concern only adult specimens. We report the hearing abilities in the dogfish Scyliorhinus canicula at different stages, from embryos that still have their yolk sac inside their egg, to juveniles. Hearing development corresponds to an increase in the frequency range from 100-300 Hz in early pre-hatching stages to 100-600 Hz in juveniles. Modifications in hearing abilities correspond to the development of the brain, the increase of the volume of the membranous labyrinth, the growth of the sensory epithelium, and the development of stereocilia in addition to kinocilium before hatching. This work offers solid insights into the development of hearing abilities that usually can only be inferred from the anatomy of vertebrates or after birth/hatching. It shows also that shark can be sensitive to background noise during development.

Local sonic activity reveals potential partitioning in a coral reef fish community.

How vocal organisms share acoustic space has primarily received attention in terrestrial environments. Comparable studies in marine environments, however, remain rare. By recording sounds on a coral reef in French Polynesia for 48 h and 24 h, this study provides first insights on how different sound types are distributed within the acoustic space and may create acoustic niches optimizing acoustic communication within a highly diverse community containing numerous soniferous fish species. Day-time was dominated by two to six sound types, while recordings performed at night revealed a more diverse vocal community made of up to nineteen sound types. Calling activity was distributed over time allowing each sound type to dominate the soundscape sequentially. Additionally, differences in the acoustic features of sounds occurring during the same period were observed. Such partitioning in time and acoustic spaces would reduce potential overlaps of sounds produced by vocal species living in sympatry in coral reefs.

Mass mortality in a Marine Educational Area on a remote South Pacific Atoll.

In 2018, on the isolated Anaa atoll (South Pacific), a Marine Educational Area (MEA) was established by the local community to protect fisheries resources on the reef barrier next to their village. Whilst the remote location of the small MEA has provided some protection from anthropogenic pressures due to distance and low population, we showed that from 26 to 27 November 2018, high temperatures along with a hypoxic event and a low tide led to the mass mortality of several Anaa's marine species. The mass mortality in the MEA (area: 27,000 m2) included >14,000 juvenile fish, 1300 adult fish, 5100 juvenile crustaceans, and 260 juvenile octopus. This finding is particularly concerning because despite the creation of a MEA to protect marine resources, impacts from the warming waters associated with climate change limited the local efforts in Anaa atoll. This small, focused study demonstrates that local intervention may not be enough to mitigate the large-scale impacts of global climate change. It notes that local intervention can directly improve the fisheries resource but must be placed within a context of national and global interventions on climate change.

Effects of Asparagopsis taxiformis metabolites on the feeding behaviour of post-larval Acanthurus triostegus.

Our study highlights the effect of the macroalgae Asparagopsis taxiformis on the feeding behaviour of the tropical surgeonfish Acanthurus triostegus. The presence of A. taxiformis chemical cues reduced A. triostegus feeding, suggesting that the presence of this algae could affect not only the survival of fish in the post-larval stage, but also alter the grazing pressure on coral reefs.

Simultaneous production of two kinds of sounds in relation with sonic mechanism in the boxfish Ostracion meleagris and O. cubicus.

In fishes, sonic abilities for communication purpose usually involve a single mechanism. We describe here the sonic mechanism and sounds in two species of boxfish, the spotted trunkfish Ostracion meleagris and the yellow boxfish Ostracion cubicus. The sonic mechanism utilizes a T-shaped swimbladder with a swimbladder fenestra and two separate sonic muscle pairs. Extrinsic vertical muscles attach to the vertebral column and the swimbladder. Perpendicularly and below these muscles, longitudinal intrinsic muscles cover the swimbladder fenestra. Sounds are exceptional since they are made of two distinct types produced in a sequence. In both species, humming sounds consist of long series (up to 45 s) of hundreds of regular low-amplitude pulses. Hums are often interspersed with irregular click sounds with an amplitude that is ten times greater in O. meleagris and forty times greater in O. cubicus. There is no relationship between fish size and many acoustic characteristics because muscle contraction rate dictates the fundamental frequency. We suggest that hums and clicks are produced by either separate muscles or by a combination of the two. The mechanism complexity supports an investment of boxfish in this communication channel and underline sounds as having important functions in their way of life.

Evaluation of microplastic ingestion by tropical fish from Moorea Island, French Polynesia.

Microplastics are ubiquitous throughout the oceans, yet few studies have documented their occurrence in marine organisms associated with coral reefs. Four genera of adult fish were sampled (Myripristis spp., Siganus spp., Epinephelus merra and Cheilopogon simus) from different trophic guilds around the tropical island of Moorea, French Polynesia. Digestive tracts from 133 adult fish were surveyed and microplastics were found in 28 tracts (21%). Abundance of ingested microplastic pieces per individual fish varied from 1 to 3 pieces, with an average of 1.25 ±â€¯0.13 ingested microplastic pieces. Microplastics size ranged from 0.031 to 2.44 mm and 70% of microplastics did not exceed 0.3 mm in size. Overall, this study shows that the number and size of microplastic ingested per trophic groups are independent of trophic guild. Additional studies are needed to sample in other tropical regions in order to have a better assessment of microplastic occurrence in coral reefs.

Decreased retention of olfactory predator recognition in juvenile surgeon fish exposed to pesticide.

Dory, the animated surgeonfish created by the Pixar Animation studios, famously suffered from short-term memory loss leading to many adventures. In reality, many fishes have excellent cognitive abilities and are able to learn and retain important information such as the identity of predators. However, if and how cognition can be affected by anthropogenically altered oceanic conditions is poorly understood. Here, we examine the effect of a widely used pesticide, chlorpyrifos, on the retention of acquired predator recognition in post-larval stage of the surgeonfish Acanthurus triostegus. Through associative learning, post-larvae of A. triostegus were first observed to forage significantly less in the presence of conspecific alarm cues and alarm cues associated to a predator's odor. The retention of this anti-predator behavior was estimated to last between 2 and 5 days in the absence of pesticide. However, environmentally-relevant concentrations of chlorpyrifos (1 µg.L-1) induced the loss of this acquired predator recognition. This reduced ability to recognize learned predators is discussed as it may lead to more vulnerable fish communities in coastal areas subjected to organophosphate pesticide pollution.

Boat noise prevents soundscape-based habitat selection by coral planulae.

Understanding the relationship between coral reef condition and recruitment potential is vital for the development of effective management strategies that maintain coral cover and biodiversity. Coral larvae (planulae) have been shown to use certain sensory cues to orient towards settlement habitats (e.g. the odour of live crustose coralline algae - CCA). However, the influence of auditory cues on coral recruitment, and any effect of anthropogenic noise on this process, remain largely unknown. Here, we determined the effect of protected reef (MPA), exploited reef (non-MPA) soundscapes, and a source of anthropogenic noise (boat) on the habitat preference for live CCA over dead CCA in the planula of two common Indo-Pacific coral species (Pocillopora damicornis and Acropora cytherea). Soundscapes from protected reefs significantly increased the phonotaxis of planulae of both species towards live CCA, especially when compared to boat noise. Boat noise playback prevented this preferential selection of live CCA as a settlement substrate. These results suggest that sources of anthropogenic noise such as motor boat can disrupt the settlement behaviours of coral planulae. Acoustic cues should be accounted for when developing management strategies aimed at maximizing larval recruitment to coral reefs.