Combining stereo-video monitoring and physiological trials to estimate reef fish metabolic demands in the wild.

Organismal metabolic rates (MRs) are the basis of energy and nutrient fluxes through ecosystems. In the marine realm, fishes are some of the most prominent consumers. However, their metabolic demand in the wild (field MR [FMR]) is poorly documented, because it is challenging to measure directly. Here, we introduce a novel approach to estimating the component of FMR associated with voluntary activity (i.e., the field active MR [ AM R field ] ). Our approach combines laboratory-based respirometry, swimming speeds, and field-based stereo-video systems to estimate the activity of individuals. We exemplify our approach by focusing on six coral reef fish species, for which we quantified standard MR and maximum MR (SMR and MMR, respectively) in the laboratory, and body sizes and swimming speeds in the field. Based on the relationships between MR, body size, and swimming speeds, we estimate that the activity scope (i.e., the ratio between AM R field and SMR) varies from 1.2 to 3.2 across species and body sizes. Furthermore, we illustrate that the scaling exponent for AM R field varies across species and can substantially exceed the widely assumed value of 0.75 for SMR. Finally, by scaling organismal AM R field estimates to the assemblage level, we show the potential effect of this variability on community metabolic demand. Our approach may improve our ability to estimate elemental fluxes mediated by a critically important group of aquatic animals through a non-destructive, widely applicable technique.

Biological trade-offs underpin coral reef ecosystem functioning.

Human impact increasingly alters global ecosystems, often reducing biodiversity and disrupting the provision of essential ecosystem services to humanity. Therefore, preserving ecosystem functioning is a critical challenge of the twenty-first century. Coral reefs are declining worldwide due to the pervasive effects of climate change and intensive fishing, and although research on coral reef ecosystem functioning has gained momentum, most studies rely on simplified proxies, such as fish biomass. This lack of quantitative assessments of multiple process-based ecosystem functions hinders local and regional conservation efforts. Here we combine global coral reef fish community surveys and bioenergetic models to quantify five key ecosystem functions mediated by coral reef fishes. We show that functions exhibit critical trade-offs driven by varying community structures, such that no community can maximize all functions. Furthermore, functions are locally dominated by few species, but the identity of dominant species substantially varies at the global scale. In fact, half of the 1,110 species in our dataset are functionally dominant in at least one location. Our results reinforce the need for a nuanced, locally tailored approach to coral reef conservation that considers multiple ecological functions beyond the effect of standing stock biomass.

Scaling up calcification, respiration, and photosynthesis rates of six prominent coral taxa.

Coral reefs provide a range of important services to humanity, which are underpinned by community-level ecological processes such as coral calcification. Estimating these processes relies on our knowledge of individual physiological rates and species-specific abundances in the field. For colonial animals such as reef-building corals, abundance is frequently expressed as the relative surface cover of coral colonies, a metric that does not account for demographic parameters such as coral size. This may be problematic because many physiological rates are directly related to organism size, and failure to account for linear scaling patterns may skew estimates of ecosystem functioning. In the present study, we characterize the scaling of three physiological rates - calcification, respiration, and photosynthesis - considering the colony size for six prominent, reef-building coral taxa in Mo'orea, French Polynesia. After a seven-day acclimation period in the laboratory, we quantified coral physiological rates for three hours during daylight (i.e., calcification and gross photosynthesis) and one hour during night light conditions (i.e., dark respiration). Our results indicate that area-specific calcification rates are higher for smaller colonies across all taxa. However, photosynthesis and respiration rates remain constant over the colony-size gradient. Furthermore, we revealed a correlation between the demographic dynamics of coral genera and the ratio between net primary production and calcification rates. Therefore, intraspecific scaling of reef-building coral physiology not only improves our understanding of community-level coral reef functioning but it may also explain species-specific responses to disturbances.

Thermal stress responses of the antipatharian Stichopathes sp. from the mesophotic reef of Mo'orea, French Polynesia.

Antipatharians, also called black corals, are present in almost all oceans of the world, until extreme depths. In several regions, they aggregate in higher densities to form black coral beds that support diverse animal communities and create biodiversity hotspots. These recently discovered ecosystems are currently threatened by fishing activities and illegal harvesting for commercial purposes. Despite this, studies dedicated to the physiology of antipatharians are scarce and their responses to global change stressors have remained hardly explored since recently. Here, we present the first study on the physiological responses of a mesophotic antipatharian Stichopathes sp. (70-90 m) to thermal stress through a 16-d laboratory exposure (from 26 to 30.5 °C). Oxygen consumption measurements allowed identifying the physiological tipping point of Stichopathes sp. (Topt = 28.3 °C; 2.7 °C above mean ambient condition). Our results follow theoretical predictions as performances start to decrease beyond Topt, with lowered oxygen consumption rates, impairment of the healing capacities, increased probability of tissue necrosis and stress responses activated as a function of temperature (i.e. increase in mucocyte density and total antioxidant capacity). Altogether, our work indicates that Stichopathes sp. lives at suboptimal performances during the coldest months of the year, but also that it is likely to have low acclimatization capacity and a narrow thermal breadth.

Phylogeny, body morphology, and trophic level shape intestinal traits in coral reef fishes.

Trait-based approaches are increasingly used to study species assemblages and understand ecosystem functioning. The strength of these approaches lies in the appropriate choice of functional traits that relate to the functions of interest. However, trait-function relationships are often supported by weak empirical evidence.Processes related to digestion and nutrient assimilation are particularly challenging to integrate into trait-based approaches. In fishes, intestinal length is commonly used to describe these functions. Although there is broad consensus concerning the relationship between fish intestinal length and diet, evolutionary and environmental forces have shaped a diversity of intestinal morphologies that is not captured by length alone.Focusing on coral reef fishes, we investigate how evolutionary history and ecology shape intestinal morphology. Using a large dataset encompassing 142 species across 31 families collected in French Polynesia, we test how phylogeny, body morphology, and diet relate to three intestinal morphological traits: intestinal length, diameter, and surface area.We demonstrate that phylogeny, body morphology, and trophic level explain most of the interspecific variability in fish intestinal morphology. Despite the high degree of phylogenetic conservatism, taxonomically unrelated herbivorous fishes exhibit similar intestinal morphology due to adaptive convergent evolution. Furthermore, we show that stomachless, durophagous species have the widest intestines to compensate for the lack of a stomach and allow passage of relatively large undigested food particles.Rather than traditionally applied metrics of intestinal length, intestinal surface area may be the most appropriate trait to characterize intestinal morphology in functional studies.

Juvenile corals underpin coral reef carbonate production after disturbance.

Sea-level rise is predicted to cause major damage to tropical coastlines. While coral reefs can act as natural barriers for ocean waves, their protection hinges on the ability of scleractinian corals to produce enough calcium carbonate (CaCO3 ) to keep up with rising sea levels. As a consequence of intensifying disturbances, coral communities are changing rapidly, potentially reducing community-level CaCO3 production. By combining colony-level physiology and long-term monitoring data, we show that reefs recovering from major disturbances can produce 40% more CaCO3 than currently estimated due to the disproportionate contribution of juvenile corals. However, the buffering effect of highly productive juvenile corals is compromised by recruitment failures, which have been more frequently observed after large-scale, repeated bleaching events. While the size structure of corals can bolster a critical ecological function on reefs, climate change impacts on recruitment may undermine this buffering effect, thus further compromising the persistence of reefs and their provision of important ecosystem services.

Defining Coral Bleaching as a Microbial Dysbiosis within the Coral Holobiont.

Coral microbiomes are critical to holobiont health and functioning, but the stability of host-microbial interactions is fragile, easily shifting from eubiosis to dysbiosis. The heat-induced breakdown of the symbiosis between the host and its dinoflagellate algae (that is, "bleaching"), is one of the most devastating outcomes for reef ecosystems. Yet, bleaching tolerance has been observed in some coral species. This review provides an overview of the holobiont's diversity, explores coral thermal tolerance in relation to their associated microorganisms, discusses the hypothesis of adaptive dysbiosis as a mechanism of environmental adaptation, mentions potential solutions to mitigate bleaching, and suggests new research avenues. More specifically, we define coral bleaching as the succession of three holobiont stages, where the microbiota can (i) maintain essential functions for holobiont homeostasis during stress and/or (ii) act as a buffer to mitigate bleaching by favoring the recruitment of thermally tolerant Symbiodiniaceae species (adaptive dysbiosis), and where (iii) environmental stressors exceed the buffering capacity of both microbial and dinoflagellate partners leading to coral death.

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.

Parentage analyses identify local dispersal events and sibling aggregations in a natural population of Millepora hydrocorals, a free-spawning marine invertebrate.

Dispersal is a critical process for the persistence and productivity of marine populations. For many reef species, there is increasing evidence that local demography and self-recruitment have major consequences on their genetic diversity and adaptation to environmental change. Yet empirical data of dispersal patterns in reef-building species remain scarce. Here, we document the first genetic estimates of self-recruitment and dispersal distances in a free-spawning marine invertebrate, the hydrocoral Millepora cf. platyphylla. Using twelve microsatellite markers, we gathered genotypic information from 3,160 georeferenced colonies collected over 27,000 m2 of a single reef in three adjacent habitats in Moorea, French Polynesia; the mid slope, upper slope, and back reef. Although the adult population was predominantly clonal (85% were clones), our parentage analysis revealed a moderate self-recruitment rate with a minimum of 8% of sexual propagules produced locally. Assigned offspring often settled at <10 m from their parents and dispersal events decrease with increasing geographic distance. There were no discrepancies between the dispersal distances of offspring assigned to parents belonging to clonal versus nonclonal genotypes. Interhabitat dispersal events via cross-reef transport were also detected for sexual and asexual propagules. Sibship analysis showed that full siblings recruit nearby on the reef (more than 40% settled at <30 m), resulting in sibling aggregations. Our findings highlight the importance of self-recruitment together with clonality in stabilizing population dynamics, which may ultimately enhance local sustainability and resilience to disturbance.

Spatial distribution of juvenile fish along an artificialized seascape, insights from common coastal species in the Northwestern Mediterranean Sea.

Along the littoral, a growing number of anthropogenic structures have caused substantial habitat destruction. Despite their detrimental impact, these constructions could play a role in the functioning of coastal ecosystems. The objective of this work was to assess the distribution of juvenile coastal fish along a seascape composed of various natural and artificial habitats in order to determine the potential role of coastal infrastructures as juvenile habitat. We surveyed juvenile populations on various infrastructures and natural sites along a 100 km shoreline of the French Mediterranean coast. Juvenile densities varied according to the level of artificialization of the sites. Densities were the highest on coastal defense structures, intermediate in natural sites and lowest in harbors. Focusing inside harbors revealed highly variable densities depending on the type of habitat, with densities on ripraps or jetties that were equivalent to those of natural sites. Our results underline the importance of anthropogenic structures as potential juvenile habitats, which is too often not considered in management plans.

Shallow rocky nursery habitat for fish: Spatial variability of juvenile fishes among this poorly protected essential habitat.

Coastal nursery habitats are essential for the renewal of adult fish populations. We quantified the availability of a coastal nursery habitat (shallow heterogeneous rocky bottoms) and the spatial variability of its juvenile fish populations along 250km of the Catalan coastline (France and Spain). Nurseries were present in 27% of the coastline, but only 2% of them benefited from strict protection status. For nine taxa characteristic of this habitat, total juvenile densities varied significantly between nursery sites along the coastline, with the highest densities being found on the northern sites. Recruitment level (i.e. a proxy of nursery value) was not explained by protection level, but it was moderately and positively correlated with an anthropization index. Patterns of spatial variations were taxa-specific. Exceptional observations of four juveniles of the protected grouper Epinephelus marginatus were recorded. Our data on habitat availability and recruitment levels provides important informations which help to focus MPA management efforts.

Population structure of the hydrocoral Millepora platyphylla in habitats experiencing different flow regimes in Moorea, French Polynesia.

While the fire coral Millepora platyphylla is an important component of Indo-Pacific reefs, where it thrives in a wide range of environments, the ecological and biological processes driving its distribution and population structure are not well understood. Here, we quantified this species' population structure in five habitats with contrasting hydrodynamic regimes in Moorea, French Polynesia; two in the fore reef: mid and upper slopes, and three in the lagoon: back, fringing and patch reefs. A total of 3651 colonies of fire corals were mapped and measured over 45,000 m2 of surveyed reef. Due to the species' sensitivity to fragmentation in response to strong water movement, hydrodynamic conditions (e.g. waves, pass and lagoonal circulation) corresponded to marked differences in colony size distributions, morphology and recruitment dynamics among habitats. The size structure varied among reef habitats with higher proportions of larger colonies in calm nearshore reefs (fringing and patch reefs), while populations were dominated by smaller colonies in the exposed fore reefs. The highest densities of fire corals were recorded in fore reef habitats (0.12-0.20 n.m-2) where the proportion of recruits and juveniles was higher at mid slope populations (49.3%) than on the upper slope near where waves break (29.0%). In the latter habitat, most colonies grew as vertical sheets on encrusting bases making them more vulnerable to colony fragmentation, whereas fire corals were encrusting or massive in all other habitats. The lowest densities of M. platyphylla occurred in lagoonal habitats (0.02-0.04 n.m-2) characterized by a combination of low water movement and other physical and biological stressors. This study reports the first evidence of population structure of fire corals in two common reef environments and illustrates the importance of water flow in driving population dynamic processes of these reef-building species.