David Lecchini

Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos

Larval recruitment, the transition of pelagic larvae into reef-associated juveniles, is a critical step for the resilience of marine fish populations but its molecular control is unknown. Here, we investigate whether thyroid-hormones (TH) and their receptors (TR) coordinate the larval recruitment of the coral-reef-fish Acanthurus triostegus. We demonstrate an increase of TH-levels and TR-expressions in pelagic-larvae, followed by a decrease in recruiting juveniles. We generalize these observations in four other coral reef-fish species. Treatments with TH or TR-antagonist, as well as relocation to the open-ocean, disturb A. triostegus larvae transformation and grazing activity. Likewise, chlorpyrifos, a pesticide often encountered in coral-reefs, impairs A. triostegus TH-levels, transformation, and grazing activity, hence diminishing this herbivore’s ability to control the spread of reef-algae. Larval recruitment therefore corresponds to a TH-controlled metamorphosis, sensitive to endocrine disruption. This provides a framework to understand how larval recruitment, critical to reef-ecosystems maintenance, is altered by anthropogenic stressors.

Consistency in the supply of larval fishes among coral reefs in French Polynesia

For marine fishes with a bipartite life cycle, pelagic larval dispersal can shape the distribution, connectivity, composition and resilience of adult populations. Numerous studies of larval dispersal, and associated settlement and recruitment processes, have examined the relationship between population connectivity and oceanographic features. However, relatively little is known about spatial and temporal variation in the abundance of larvae settling among different reefs and the extent to which the species assemblage of larvae settling at one location is reflective of the assemblage in neighbouring areas. Here, using crest nets, which provide a non-selective measure of the total abundance and assemblage of larvae settling to a reef (i.e. larval supply), we collected larval coral reef fishes at five locations surrounding two spatially disparate French Polynesian islands: Moorea and Nengo-Nengo. Overall, larval settlement patterns were correlated with the lunar cycle, with larval abundance peaking during the new moon. Although there were some spatial differences in larval supply among the five monitored sites, settlement patterns were largely consistent, even at the species level, irrespective of factors such as coastline orientation or distance between sites. This study provides further insights into the mechanisms driving patterns of dispersal and settlement of larval fishes over large spatial scales.

Habitat selection by marine larvae in changing chemical environments

The replenishment and persistence of marine species is contingent on dispersing larvae locating suitable habitat and surviving to a reproductive stage. Pelagic larvae rely on environmental cues to make behavioural decisions with chemical information being important for habitat selection at settlement. We explored the sensory world of crustaceans and fishes focusing on the impact anthropogenic alterations (ocean acidification, red soil, pesticide) have on conspecific chemical signals used by larvae for habitat selection. Crustacean (Stenopus hispidus) and fish (Chromis viridis) larvae recognized their conspecifics via chemical signals under control conditions. In the presence of acidified water, red soil or pesticide, the ability of larvae to chemically recognize conspecific cues was altered. Our study highlights that recruitment potential on coral reefs may decrease due to anthropogenic stressors. If so, populations of fishes and crustaceans will continue their rapid decline; larval recruitment will not replace and sustain the adult populations on degraded reefs.

Complete and rapid reversal of the body color pattern in juveniles of the convict surgeonfish Acanthurus triostegus at Moorea Island (French Polynesia)

Color polymorphism is widespread in animals and can be associated with temporary adjustments to environmental variables (phenotypic plasticity). In teleost fishes, one of the most remarkable examples of color plasticity is background adaptation in flatfishes. However, such rapid and complete changes in body color and pattern remain relatively unreported in other species. The convict surgeonfish Acanthurus triostegus is a gregarious species whose body color pattern consists of black vertical bars on a whitish body. Here, we describe an entirely reverse body color pattern (white vertical bars on a blackish body) that we observed in some A. triostegus juveniles in a nursery area at Moorea Island, French Polynesia. In aquaria, we determined that change from one color pattern to the other is rapid, reversible, and corresponds to phenotypic plasticity associated with aggressive behavior.

Exposure to agricultural pesticide impairs visual lateralization in a larval coral reef fish

Lateralization, i.e. the preferential use of one side of the body, may convey fitness benefits for organisms within rapidly-changing environments, by optimizing separate and parallel processing of different information between the two brain hemispheres. In coral reef-fishes, the movement of larvae from planktonic to reef environments (recruitment) represents a major life-history transition. This transition requires larvae to rapidly identify and respond to sensory cues to select a suitable habitat that facilitates survival and growth. This ‘recruitment’ is critical for population persistence and resilience. In aquarium experiments, larval Acanthurus triostegus preferentially used their right-eye to investigate a variety of visual stimuli. Despite this, when held in in situ cages with predators, those larvae that previously favored their left-eye exhibited higher survival. These results support the “brain’s right-hemisphere” theory, which predicts that the right-eye (i.e. left-hemisphere) is used to categorize stimuli while the left-eye (i.e. right-hemisphere) is used to inspect novel items and initiate rapid behavioral-responses. While these experiments confirm that being highly lateralized is ecologically advantageous, exposure to chlorpyrifos, a pesticide often inadvertently added to coral-reef waters, impaired visual-lateralization. This suggests that chemical pollutants could impair the brain function of larval fishes during a critical life-history transition, potentially impacting recruitment success.

Snapshot recordings provide a first description of the acoustic signatures of deeper habitats adjacent to coral reefs of Moorea

Acoustic recording has been recognized as a valuable tool for non-intrusive monitoring of the marine environment, complementing traditional visual surveys. Acoustic surveys conducted on coral ecosystems have so far been restricted to barrier reefs and to shallow depths (10–30 m). Since they may provide refuge for coral reef organisms, the monitoring of outer reef slopes and describing of the soundscapes of deeper environment could provide insights into the characteristics of different biotopes of coral ecosystems. In this study, the acoustic features of four different habitats, with different topographies and substrates, located at different depths from 10 to 100 m, were recorded during day-time on the outer reef slope of the north Coast of Moorea Island (French Polynesia). Barrier reefs appeared to be the noisiest habitats whereas the average sound levels at other habitats decreased with their distance from the reef and with increasing depth. However, sound levels were higher than expected by propagation models, supporting that these habitats possess their own sound sources. While reef sounds are known to attract marine larvae, sounds from deeper habitats may then also have a non-negligible attractive potential, coming into play before the reef itself.

Sound production mechanism in triggerfish (Balistidae): a synapomorphy

ABSTRACT The ability to produce sounds for acoustic communication is known in different Balistidae species but the eventual synapomorphic aspect of the mechanism remains to be shown. In Rhinecanthus aculeatus, sounds result from alternate sweeping movements of the right and left pectoral fins, which push a system of three scutes against the swim bladder wall. In this study, we made a comparison between the sounds produced by this species and two additional ones (Balistapus undulatus and Rhinecanthus rectangulus) using hand-held specimens to provide a description of the sound mechanism. The results highlighted that the sound production mechanism is similar in the three species. According to recent phylogenetic data and shared morphological features, this mechanism could be common to the majority of Balistidae family members and all species could be capable of sound production using pectoral fins. Summary: Comparison of sounds and morphology combined with current data on Balistidae phylogeny support the suggestion that all the family members should be capable of sound production using their pectoral fins.

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.

Taxonomic validation of Encheliophis chardewalli with description of calling abilities

Encheliophis chardewalli was described from a single cleared and stained specimen. Twelve years later, additional specimens were found in the lagoon of Moorea (French Polynesia) in association with their host, the sea cucumber Actinopyga mauritiana. These fish were used to consolidate the species diagnosis, to validate species status and to record sound production. This species is remarkable because of its ability to penetrate inside the cloaca of sea cucumbers having anal teeth and the fact this species is largely unknown despite it lives in lagoons in 1m depth. Encheliophis chardewalli produced three sound types: long regular calls made of trains of numerous pulses, short irregular calls characterized by a constant lowering of its pulse period and short regular call (or knock) made of 3 to 6 pulses. Comparison with other sympatric Carapini supports a large and distinct repertoire. Morphological characteristics could be the result of reduced body size allowing to penetrate inside a new host, thus avoiding competition and conflict with other larger sympatric Carapini species.

Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes

BackgroundBiologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. However, the origins and evolution of this diversity are still poorly understood. Disentangling the evolution of simple color patterns offers the opportunity to dissect both ultimate and proximate causes underlying color diversity.ResultsHere, we study clownfishes, a tribe of 30 species within the Pomacentridae that displays a relatively simple color pattern made of zero to three vertical white stripes on a dark body background. Mapping the number of white stripes on the evolutionary tree of clownfishes reveals that their color pattern diversification results from successive caudal to rostral losses of stripes. Moreover, we demonstrate that stripes always appear with a rostral to caudal stereotyped sequence during larval to juvenile transition. Drug treatments (TAE 684) during this period leads to a dose-dependent loss of stripes, demonstrating that white stripes are made of iridophores and that these cells initiate the stripe formation. Surprisingly, juveniles of several species (e.g., Amphiprion frenatus) have supplementary stripes when compared to their respective adults. These stripes disappear caudo-rostrally during the juvenile phase leading to the definitive color pattern. Remarkably, the reduction of stripe number over ontogeny matches the sequences of stripe losses during evolution, showing that color pattern diversification among clownfish lineages results from changes in developmental processes. Finally, we reveal that the diversity of striped patterns plays a key role for species recognition.ConclusionsOverall, our findings illustrate how developmental, ecological, and social processes have shaped the diversification of color patterns during the radiation of an emblematic coral reef fish lineage.