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.

Rare species support vulnerable functions in high-diversity ecosystems.

Around the world, the human-induced collapses of populations and species have triggered a sixth mass extinction crisis, with rare species often being the first to disappear. Although the role of species diversity in the maintenance of ecosystem processes has been widely investigated, the role of rare species remains controversial. A critical issue is whether common species insure against the loss of functions supported by rare species. This issue is even more critical in species-rich ecosystems where high functional redundancy among species is likely and where it is thus often assumed that ecosystem functioning is buffered against species loss. Here, using extensive datasets of species occurrences and functional traits from three highly diverse ecosystems (846 coral reef fishes, 2,979 alpine plants, and 662 tropical trees), we demonstrate that the most distinct combinations of traits are supported predominantly by rare species both in terms of local abundance and regional occupancy. Moreover, species that have low functional redundancy and are likely to support the most vulnerable functions, with no other species carrying similar combinations of traits, are rarer than expected by chance in all three ecosystems. For instance, 63% and 98% of fish species that are likely to support highly vulnerable functions in coral reef ecosystems are locally and regionally rare, respectively. For alpine plants, 32% and 89% of such species are locally and regionally rare, respectively. Remarkably, 47% of fish species and 55% of tropical tree species that are likely to support highly vulnerable functions have only one individual per sample on average. Our results emphasize the importance of rare species conservation, even in highly diverse ecosystems, which are thought to exhibit high functional redundancy. Rare species offer more than aesthetic, cultural, or taxonomic diversity value; they disproportionately increase the potential breadth of functions provided by ecosystems across spatial scales. As such, they are likely to insure against future uncertainty arising from climate change and the ever-increasing anthropogenic pressures on ecosystems. Our results call for a more detailed understanding of the role of rarity and functional vulnerability in ecosystem functioning.

Challenging trophic position assessments in complex ecosystems: Calculation method, choice of baseline, trophic enrichment factors, season and feeding guild do matter: A case study from Marquesas Islands coral reefs.

Assessments of ecosystem functioning are a fundamental ecological challenge and an essential foundation for ecosystem-based management. Species trophic position (TP) is essential to characterize food web architecture. However, despite the intuitive nature of the concept, empirically estimating TP is a challenging task due to the complexity of trophic interaction networks. Various methods are proposed to assess TPs, including using different sources of organic matter at the base of the food web (the 'baseline'). However, it is often not clear which methodological approach and which baseline choices are the most reliable. Using an ecosystem-wide assessment of a tropical reef (Marquesas Islands, with available data for 70 coral reef invertebrate and fish species), we tested whether different commonly used TP estimation methods yield similar results and, if not, whether it is possible to identify the most reliable method. We found significant differences in TP estimates of up to 1.7 TPs for the same species, depending on the method and the baseline used. When using bulk stable isotope data, the choice of the baseline significantly impacted TP values. Indeed, while nitrogen stable isotope (δ15N) values of macroalgae led to consistent TP estimates, those using phytoplankton generated unrealistically low TP estimates. The use of a conventional enrichment factor (i.e. 3.4‰) or a 'variable' enrichment factor (i.e. according to feeding guilds) also produced clear discrepancies between TP estimates. TPs obtained with δ15N values of source amino acids (compound-specific isotope analysis) were close to those assessed with macroalgae. An opposite seasonal pattern was found, with significantly lower TPs in winter than in summer for most species, with particularly pronounced differences for lower TP species. We use the observed differences to discuss possible drivers of the diverging TP estimates and the potential ecological implications.

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.

Multi-trophic markers illuminate the understanding of the functioning of a remote, low coral cover Marquesan coral reef food web.

We studied the food web structure and functioning of a coral reef ecosystem in the Marquesas Islands, French Polynesia, characterized by low coral cover, high sea surface temperature and meso- to eutrophic waters. The Marquesas constitute a relevant ecosystem to understand the functioning of low diversity reefs that are also subject to global change. A multi-tracer assessment of organic matter pathways was run to delineate ecosystem functioning, using analysis of fatty acids, bulk and compound specific stable isotope analysis and stable isotopes mixing models. Macroalgae and phytoplankton were the two major food sources fueling this food web with, however, some marked seasonal variations. Specifically, zooplankton relied on phytoplankton-derived organic matter and herbivorous fishes on macroalgae-derived organic matter to a much higher extent in summer than in winter (~ 75% vs. ~ 15%, and ~ 70 to 75% vs. ~ 5 to 15%, respectively) . Despite remarkably high δ15N values for all trophic compartments, likely due to local dynamics in the nitrogen stock, trophic levels of consumers were similar to those of other coral reef ecosystems. These findings shed light on the functioning of low coral cover systems, which are expected to expand worldwide under global change.

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.

Individual back-calculated size-at-age based on otoliths from Pacific coral reef fish species.

Somatic growth is a critical biological trait for organismal, population, and ecosystem-level processes. Due to its direct link with energetic demands, growth also represents an important parameter to estimate energy and nutrient fluxes. For marine fishes, growth rate information is most frequently derived from sagittal otoliths, and most of the available data stems from studies on temperate species that are targeted by commercial fisheries. Although the analysis of otoliths is a powerful tool to estimate individual growth, the time-consuming nature of otolith processing is one barrier for collection of comprehensive datasets across multiple species. This is especially true for coral reef fishes, which are extremely diverse. Here, we provide back-calculated size-at-age estimates (including measures of uncertainty) based on sagittal otoliths from 710 individuals belonging to 45 coral reef fish species from French Polynesia. In addition, we provide Von Bertalanffy growth parameters which are useful to predict community level biomass production.

Hierarchical drivers of reef-fish metacommunity structure.

Coral reefs are highly complex ecological systems, where multiple processes interact across scales in space and time to create assemblages of exceptionally high biodiversity. Despite the increasing frequency of hierarchically structured sampling programs used in coral-reef science, little progress has been made in quantifying the relative importance of processes operating across multiple scales. The vast majority of reef studies are conducted, or at least analyzed, at a single spatial scale, ignoring the implicitly hierarchical structure of the overall system in favor of small-scale experiments or large-scale observations. Here we demonstrate how alpha (mean local number of species), beta diversity (degree of species dissimilarity among local sites), and gamma diversity (overall species richness) vary with spatial scale, and using a hierarchical, information-theoretic approach, we evaluate the relative importance of site-, reef-, and atoll-level processes driving the fish metacommunity structure among 10 atolls in French Polynesia. Process-based models, representing well-established hypotheses about drivers of reef-fish community structure, were assembled into a candidate set of 12 hierarchical linear models. Variation in fish abundance, biomass, and species richness were unevenly distributed among transect, reef, and atoll levels, establishing the relative contribution of variation at these spatial scales to the structure of the metacommunity. Reef-fish biomass, species richness, and the abundance of most functional-groups corresponded primarily with transect-level habitat diversity and atoll-lagoon size, whereas detritivore and grazer abundances were largely correlated with potential covariates of larval dispersal. Our findings show that (1) within-transect and among-atoll factors primarily drive the relationship between alpha and gamma diversity in this reef-fish metacommunity; (2) habitat is the primary correlate with reef-fish metacommunity structure at multiple spatial scales; and (3) inter-atoll connectedness was poorly correlated with the nonrandom clustering of reef-fish species. These results demonstrate the importance of modeling hierarchical data and processes in understanding reef-fish metacommunity structure.

Multiple parasite introduction and host management plan: case study of lutjanid fish in the Hawaiian Archipelago.

The bluestriped snapper Lutjanus kasmira and the blacktail snapper L. fulvus were deliberately introduced in the Hawaiian Archipelago from French Polynesia in the late 1950s to enhance local fisheries. These species rapidly spread all over the Windward Islands, became extremely abundant and, therefore, caused controversial environmental concerns. A comparison of the whole metazoan parasite community of L. kasmira and L. fulvus was performed between their native ranges in French Polynesia (Moorea Island in the Society Archipelago and Ua Huka in the Marquesas Islands) and their introduced range in O'ahu, Hawaii, USA. We suggest that 8 monogenean species have been introduced with L. kasmira and L. fulvus into the Hawaiian Archipelago from French Polynesia; 2 other species as well as one nematode should be referred to as cryptogenic. Moreover, experimental mortality conducted on monogeneans found in Polynesia emphasizes the inefficiency of anti-parasite treatment which was performed 50 yr ago, explaining possible parasite introduction. Finally, we discuss the potential threat of exotic parasites to the native fish community in the Hawaiian Archipelago and conclude that the absence of co-evolved hosts prevents parasite transfer from non-indigenous to native fishes as monogeneans are highly specific.

A DNA barcode reference library of French Polynesian shore fishes.

The emergence of DNA barcoding and metabarcoding opened new ways to study biological diversity, however, the completion of DNA barcode libraries is fundamental for such approaches to succeed. This dataset is a DNA barcode reference library (fragment of Cytochrome Oxydase I gene) for 2,190 specimens representing at least 540 species of shore fishes collected over 10 years at 154 sites across the four volcanic archipelagos of French Polynesia; the Austral, Gambier, Marquesas and Society Islands, a 5,000,000 km2 area. At present, 65% of the known shore fish species of these archipelagoes possess a DNA barcode associated with preserved, photographed, tissue sampled and cataloged specimens, and extensive collection locality data. This dataset represents one of the most comprehensive DNA barcoding efforts for a vertebrate fauna to date. Considering the challenges associated with the conservation of coral reef fishes and the difficulties of accurately identifying species using morphological characters, this publicly available library is expected to be helpful for both authorities and academics in various fields.

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.

Environmental determinants of coral reef fish diversity across several French Polynesian atolls.

The present study aimed at exploring the diversity of coral reef fishes in 10 French Polynesian atolls and sought to determine which environmental variables best explain diversity. A total of 136,614 fish belonging to 302 species were recorded in 1995 and 1996. The stepwise multiple regression analysis showed that the best model of variation in species richness (55% of total variation) incorporated three geomorphologic descriptors (atoll perimeter, submerged rim and abundance of pinnacles) and two habitat descriptors (percentage cover of dead coral and sand). The best model of variation in Shannon-Wiener's species diversity index (43% of total variation) included two geomorphologic descriptors (mean depth and level of water exchange) and three habitat descriptors (percentage cover of mud, dead coral and gravel). Overall, our survey recognises the importance of both geomorphologic and habitat descriptors as leading contenders in explaining biodiversity in relation to energy input and habitat area hypothesis.

Spinal deformities in the black-striped pipefish Syngnathus abaster (Pisces, Syngnathidae) from the Tunis North Lake, Tunisia.

Spinal deformities are seen in fishes. Deformities in the family Syngnathidae is rarely reported. Spine curvatures in natural population of pipefish, Syngnathus abaster are reported from the Tunis North Lake. The species is euryhaline and occurs along the Mediterranean coasts. Four hundred specimens of S. abaster were collected from January 2006 to December 2007 from the Tunis North Lake. Two specimens with skeletal abnormalities were described for the first time. X-rays radiographies revealed several vertebral deformities for each deformed specimen, especially at five curvation places of the caudal part. Several factors are believed to be the cause of spinal deformities of S. abaster in the Tunis North Lake, such as environmental disturbances, parasitism infection and nutritional factors.

Host introduction and parasites: a case study on the parasite community of the peacock grouper Cephalopholis argus (Serranidae) in the Hawaiian Islands.

The peacock grouper (Cephalopholis argus) was intentionally introduced to the Hawaiian coastal waters 50 years ago to enhance the local fisheries. Following introduction, this species spread rapidly and became extremely abundant. A comparison of the metazoan parasite community of C. argus was performed between its native range (Moorea Island, French Polynesia) and its introduced range (Oahu and Big Island, Hawaii). Polynesian groupers were infected with a highly diversified parasite community whereas Hawaiian groupers exhibited a depauperate ensemble of parasite species, C. argus having lost most of the parasites common in their native range. Interestingly, the grouper has not acquired new parasites present in Hawaiian waters. This study provides the first field evidence of significant parasite release in a wild but previously introduced fish in coral reefs and is discussed in relation to the Enemy-Release Hypothesis which has never been assessed in those ecosystems.

Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems.

Coral reefs have emerged as one of the ecosystems most vulnerable to climate variation and change. While the contribution of a warming climate to the loss of live coral cover has been well documented across large spatial and temporal scales, the associated effects on fish have not. Here, we respond to recent and repeated calls to assess the importance of local management in conserving coral reefs in the context of global climate change. Such information is important, as coral reef fish assemblages are the most species dense vertebrate communities on earth, contributing critical ecosystem functions and providing crucial ecosystem services to human societies in tropical countries. Our assessment of the impacts of the 1998 mass bleaching event on coral cover, reef structural complexity, and reef associated fishes spans 7 countries, 66 sites and 26 degrees of latitude in the Indian Ocean. Using Bayesian meta-analysis we show that changes in the size structure, diversity and trophic composition of the reef fish community have followed coral declines. Although the ocean scale integrity of these coral reef ecosystems has been lost, it is positive to see the effects are spatially variable at multiple scales, with impacts and vulnerability affected by geography but not management regime. Existing no-take marine protected areas still support high biomass of fish, however they had no positive affect on the ecosystem response to large-scale disturbance. This suggests a need for future conservation and management efforts to identify and protect regional refugia, which should be integrated into existing management frameworks and combined with policies to improve system-wide resilience to climate variation and change.

Larval sensory abilities and mechanisms of habitat selection of a coral reef fish during settlement.

Sensory abilities and preferences exhibited by mobile larvae during their transition to juvenile habitats can establish spatial heterogeneity that drives subsequent species interactions and dynamics of populations. We conducted a series of laboratory and field experiments using coral reef fish larvae (Chromis viridis) to determine: ecological determinants of settlement choice (conspecifics vs. heterospecifics vs. coral substrates); sensory mechanisms (visual, acoustic/vibratory, olfactory) underlying settlement choice; and sensory abilities (effective detection distances of habitat) under field conditions. C. viridis larvae responded positively to visual, acoustic/vibratory, and olfactory cues expressed by conspecifics. Overall, larvae chose compartments of experimental arenas containing conspecifics in 75% of trials, and failed to show any significant directional responses to heterospecifics or coral substrates. In field trials, C. viridis larvae detected reefs containing conspecifics using visual and/or acoustic/vibratory cues at distances <75 cm; detection distances increased to <375 cm when olfactory capacity was present (particularly for reefs located up-current). We conducted high performance liquid chromatography (HPLC) analyses of seawater containing C. viridis juveniles and isolated high concentrations of several organic compounds. Subsequent laboratory trials demonstrated that C. viridis larvae responded positively to only one of these organic compounds. This compound was characterized by a weak polarity and was detected at 230 nm with a 31-min retention time in HPLC. Overall, our results suggest that fishes may use a range of sensory mechanisms effective over different spatial scales to detect and choose settlement sites, and species-specific cues may play a vital role in establishment of spatial patterns at settlement.