Functional changes across marine habitats due to ocean acidification.

Global environmental change drives diversity loss and shifts in community structure. A key challenge is to better understand the impacts on ecosystem function and to connect species and trait diversity of assemblages with ecosystem properties that are in turn linked to ecosystem functioning. Here we quantify shifts in species composition and trait diversity associated with ocean acidification (OA) by using field measurements at marine CO2 vent systems spanning four reef habitats across different depths in a temperate coastal ecosystem. We find that both species and trait diversity decreased, and that ecosystem properties (understood as the interplay between species, traits, and ecosystem function) shifted with acidification. Furthermore, shifts in trait categories such as autotrophs, filter feeders, herbivores, and habitat-forming species were habitat-specific, indicating that OA may produce divergent responses across habitats and depths. Combined, these findings reveal the importance of connecting species and trait diversity of marine benthic habitats with key ecosystem properties to anticipate the impacts of global environmental change. Our results also generate new insights on the predicted general and habitat-specific ecological consequences of OA.

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.

Shift and homogenization of gut microbiome during invasion in marine fishes.

Biological invasion is one of the main components of global changes in aquatic ecosystems. Unraveling how establishment in novel environments affects key biological features of animals is a key step towards understanding invasion. Gut microbiome of herbivorous animals is important for host health but has been scarcely assessed in invasive species. Here, we characterized the gut microbiome of two invasive marine herbivorous fishes (Siganus rivulatus and Siganus luridus) in their native (Red Sea) and invaded (Mediterranean Sea) ranges. The taxonomic and phylogenetic diversity of the microbiome increased as the fishes move away from the native range and its structure became increasingly different from the native microbiome. These shifts resulted in homogenization of the microbiome in the invaded range, within and between the two species. The shift in microbial diversity was associated with changes in its functions related with the metabolism of short-chain fatty acids. Altogether, our results suggest that the environmental conditions encountered by Siganidae during their expansion in Mediterranean ecosystems strongly modifies the composition of their gut microbiome along with its putative functions. Further studies should pursue to identify the precise determinants of these modifications (e.g. changes in host diet or behavior, genetic differentiation) and whether they participate in the ecological success of these species.

An invasive herbivorous fish (Siganus rivulatus) influences both benthic and planktonic microbes through defecation and nutrient excretion.

Direct and indirect impacts by invasive animals on plants and other animals through predation and competition have been evidenced in many ecosystems. For instance, the rabbitfish Siganus rivulatus, originating from the Red Sea, is now the most abundant species in costal habitats of South-Eastern Mediterranean Sea where it overgrazes algae. However, little is known about its impacts on microbes through release of metabolic wastes and feces. We used a mesocosm experiment to test the effect of S. rivulatus on planktonic and benthic microbial communities. Excretion of dissolved nutrients by fish resulted in higher concentrations of dissolved inorganic nitrogen (NH4, NO2/NO3). This increase in availability of N was associated with higher N content in macroalgae, higher biomass of phytoplankton, higher abundance of bacterioplankton and shift in the structure of planktonic bacterial communities. The feces released mostly under the shelters where the fish rest at night, led to significant increases in diversity of sediment bacterial communities and shifts in their structure. The impact of S. rivulatus on planktonic microbes was related to the indirect bottom-up effect induced by excreted dissolved nutrients while its effect on benthic microbes was due to the direct release of both organic matter and microbes present in feces. Overall, this first evidence of the impacts of invasive species on planktonic and benthic microbes highlights that ongoing changes in fish biodiversity could have ecosystem-wide consequences.

Linking key human-environment theories to inform the sustainability of coral reefs.

Effective solutions to the ongoing "coral reef crisis" will remain limited until the underlying drivers of coral reef degradation are better understood. Here, we conduct a global-scale study of how four key metrics of ecosystem states and processes on coral reefs (top predator presence, reef fish biomass, trait diversity, and parrotfish scraping potential) are explained by 11 indicators based on key human-environment theories from the social sciences. Our global analysis of >1,500 reefs reveals three key findings. First, the proximity of the nearest market has the strongest and most consistent relationships with these ecosystem metrics. This finding is in keeping with a body of terrestrial research on how market accessibility shapes agricultural practices, but the integration of these concepts in marine systems is nascent. Second, our global study shows that resource conditions tend to display a n-shaped relationship with socioeconomic development. Specifically, the probabilities of encountering a top predator, fish biomass, and fish trait diversity were highest where human development was moderate but lower where development was either high or low. This finding contrasts with previous regional-scale research demonstrating an environmental Kuznets curve hypothesis (which predicts a U-shaped relationship between socioeconomic development and resource conditions). Third, together, our ecosystem metrics are best explained by the integration of different human-environment theories. Our best model includes the interactions between indicators from different theoretical perspectives, revealing how marine reserves can have different outcomes depending on how far they are from markets and human settlements, as well as the size of the surrounding human population.

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.

Ranking the biases: The choice of OTUs vs. ASVs in 16S rRNA amplicon data analysis has stronger effects on diversity measures than rarefaction and OTU identity threshold.

Advances in the analysis of amplicon sequence datasets have introduced a methodological shift in how research teams investigate microbial biodiversity, away from sequence identity-based clustering (producing Operational Taxonomic Units, OTUs) to denoising methods (producing amplicon sequence variants, ASVs). While denoising methods have several inherent properties that make them desirable compared to clustering-based methods, questions remain as to the influence that these pipelines have on the ecological patterns being assessed, especially when compared to other methodological choices made when processing data (e.g. rarefaction) and computing diversity indices. We compared the respective influences of two widely used methods, namely DADA2 (a denoising method) vs. Mothur (a clustering method) on 16S rRNA gene amplicon datasets (hypervariable region v4), and compared such effects to the rarefaction of the community table and OTU identity threshold (97% vs. 99%) on the ecological signals detected. We used a dataset comprising freshwater invertebrate (three Unionidae species) gut and environmental (sediment, seston) communities sampled in six rivers in the southeastern USA. We ranked the respective effects of each methodological choice on alpha and beta diversity, and taxonomic composition. The choice of the pipeline significantly influenced alpha and beta diversities and changed the ecological signal detected, especially on presence/absence indices such as the richness index and unweighted Unifrac. Interestingly, the discrepancy between OTU and ASV-based diversity metrics could be attenuated by the use of rarefaction. The identification of major classes and genera also revealed significant discrepancies across pipelines. Compared to the pipeline's effect, OTU threshold and rarefaction had a minimal impact on all measurements.

Phylogenetic conservatism drives nutrient dynamics of coral reef fishes.

The relative importance of evolutionary history and ecology for traits that drive ecosystem processes is poorly understood. Consumers are essential drivers of nutrient cycling on coral reefs, and thus ecosystem productivity. We use nine consumer "chemical traits" associated with nutrient cycling, collected from 1,572 individual coral reef fishes (178 species spanning 41 families) in two biogeographic regions, the Caribbean and Polynesia, to quantify the relative importance of phylogenetic history and ecological context as drivers of chemical trait variation on coral reefs. We find: (1) phylogenetic relatedness is the best predictor of all chemical traits, substantially outweighing the importance of ecological factors thought to be key drivers of these traits, (2) phylogenetic conservatism in chemical traits is greater in the Caribbean than Polynesia, where our data suggests that ecological forces have a greater influence on chemical trait variation, and (3) differences in chemical traits between regions can be explained by differences in nutrient limitation associated with the geologic context of our study locations. Our study provides multiple lines of evidence that phylogeny is a critical determinant of contemporary nutrient dynamics on coral reefs. More broadly our findings highlight the utility of evolutionary history to improve prediction in ecosystem ecology.

Microbial Shift in the Enteric Bacteriome of Coral Reef Fish Following Climate-Driven Regime Shifts.

Replacement of coral by macroalgae in post-disturbance reefs, also called a "coral-macroalgal regime shift", is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions.

Use of environmental DNA in assessment of fish functional and phylogenetic diversity.

Assessing the impact of global changes and protection effectiveness is a key step in monitoring marine fishes. Most traditional census methods are demanding or destructive. Nondisturbing and nonlethal approaches based on video and environmental DNA are alternatives to underwater visual census or fishing. However, their ability to detect multiple biodiversity factors beyond traditional taxonomic diversity is still unknown. For bony fishes and elasmobranchs, we compared the performance of eDNA metabarcoding and long-term remote video to assess species' phylogenetic and functional diversity. We used 10 eDNA samples from 30 L of water each and 25 hr of underwater videos over 4 days on Malpelo Island (pacific coast of Colombia), a remote marine protected area. Metabarcoding of eDNA detected 66% more molecular operational taxonomic units (MOTUs) than species on video. We found 66 and 43 functional entities with a single eDNA marker and videos, respectively, and higher functional richness for eDNA than videos. Despite gaps in genetic reference databases, eDNA also detected a higher fish phylogenetic diversity than videos; accumulation curves showed how 1 eDNA transect detected as much phylogenetic diversity as 25 hr of video. Environmental DNA metabarcoding can be used to affordably, efficiently, and accurately census biodiversity factors in marine systems. Although taxonomic assignments are still limited by species coverage in genetic reference databases, use of MOTUs highlights the potential of eDNA metabarcoding once reference databases have expanded.

Uso de ADN Ambiental en la Evaluación de la Diversidad Funcional y Filogenética de los Peces Resumen La evaluación del impacto de los cambios globales y la efectividad de la protección es un paso fundamental para el monitoreo de peces marinos. La mayoría de los métodos tradicionales de censos son demandantes o destructivos, por lo que las estrategias no letales y no intrusivas basadas en videograbaciones y en el ADN ambiental (ADNa) son alternativas a los censos visuales submarinos y a la pesca. Sin embargo, todavía no se conoce la habilidad que tienen estos métodos para detectar diferentes factores de la biodiversidad más allá de la diversidad taxonómica. Para los peces óseos y los elasmobranquios, comparamos el desempeño de la caracterización genética con ADNa y del video remoto de larga duración para evaluar la diversidad funcional y filogenética de las especies. Usamos diez muestras de ADNa tomadas de 30 litros de agua cada una y 25 horas de vídeos submarinos grabados durante cuatro días en la Isla Malpelo (costa del Pacífico de Colombia), un área marina protegida remota. La caracterización genética con el ADNa detectó 66% más unidades taxonómicas moleculares operacionales (UTMOs) que el video. Encontramos 66 y 43 entidades funcionales con un solo marcador de ADNa y con el video, respectivamente, y una riqueza funcional más alta para el ADNa que el video. A pesar de los vacíos en las bases de datos genéticos usadas como referencia, el ADNa también detectó una diversidad filogenética más alta que aquella en los videos; las curvas de acumulación mostraron cómo un solo transecto de ADNa detectó tanta diversidad filogenética como 25 horas de video. La caracterización genética con ADN ambiental puede usarse para censar los factores de biodiversidad de manera asequible, eficiente y certera en los sistemas marinos. Aunque las atribuciones taxonómicas todavía están limitadas por la cobertura de especies en las bases de datos genéticos de referencia, el uso de los UTMOs resalta el potencial que tiene la caracterización genética con ADNa una vez que las bases de datos de referencia sean expandidas.

The dimensionality and structure of species trait spaces.

Trait-based ecology aims to understand the processes that generate the overarching diversity of organismal traits and their influence on ecosystem functioning. Achieving this goal requires simplifying this complexity in synthetic axes defining a trait space and to cluster species based on their traits while identifying those with unique combinations of traits. However, so far, we know little about the dimensionality, the robustness to trait omission and the structure of these trait spaces. Here, we propose a unified framework and a synthesis across 30 trait datasets representing a broad variety of taxa, ecosystems and spatial scales to show that a common trade-off between trait space quality and operationality appears between three and six dimensions. The robustness to trait omission is generally low but highly variable among datasets. We also highlight invariant scaling relationships, whatever organismal complexity, between the number of clusters, the number of species in the dominant cluster and the number of unique species with total species richness. When species richness increases, the number of unique species saturates, whereas species tend to disproportionately pack in the richest cluster. Based on these results, we propose some rules of thumb to build species trait spaces and estimate subsequent functional diversity indices.

Trait similarity in reef fish faunas across the world's oceans.

Species' traits, rather than taxonomic identities, determine community assembly and ecosystem functioning, yet biogeographic patterns have been far less studied for traits. While both environmental conditions and evolutionary history shape trait biogeography, their relative contributions are largely unknown for most organisms. Here, we explore the global biogeography of reef fish traits for 2,786 species from 89 ecoregions spanning eight marine realms with contrasting environmental conditions and evolutionary histories. Across realms, we found a common structure in the distribution of species traits despite a 10-fold gradient in species richness, with a defined "backbone" of 21 trait combinations shared by all realms globally, both temperate and tropical. Across ecoregions, assemblages under similar environmental conditions had similar trait compositions despite hosting drastically different species pools from separate evolutionary lineages. Thus, despite being separated by thousands of kilometers and millions of years of evolution, similar environments host similar trait compositions in reef fish assemblages worldwide. Our findings suggest that similar trait-based management strategies can be applied among regions with distinct species pools, potentially improving conservation outcomes across diverse jurisdictions.

Human impacts on global freshwater fish biodiversity.

Freshwater fish represent one-fourth of the world's vertebrates and provide irreplaceable goods and services but are increasingly affected by human activities. A new index, Cumulative Change in Biodiversity Facets, revealed marked changes in biodiversity in >50% of the world's rivers covering >40% of the world's continental surface and >37% of the world's river length, whereas <14% of the world's surface and river length remain least impacted. Present-day rivers are more similar to each other and have more fish species with more diverse morphologies and longer evolutionary legacies. In temperate rivers, where the impact has been greatest, biodiversity changes were primarily due to river fragmentation and introduction of non-native species.

Author Correction: A new method to control error rates in automated species identification with deep learning algorithms.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A new method to control error rates in automated species identification with deep learning algorithms.

Processing data from surveys using photos or videos remains a major bottleneck in ecology. Deep Learning Algorithms (DLAs) have been increasingly used to automatically identify organisms on images. However, despite recent advances, it remains difficult to control the error rate of such methods. Here, we proposed a new framework to control the error rate of DLAs. More precisely, for each species, a confidence threshold was automatically computed using a training dataset independent from the one used to train the DLAs. These species-specific thresholds were then used to post-process the outputs of the DLAs, assigning classification scores to each class for a given image including a new class called "unsure". We applied this framework to a study case identifying 20 fish species from 13,232 underwater images on coral reefs. The overall rate of species misclassification decreased from 22% with the raw DLAs to 2.98% after post-processing using the thresholds defined to minimize the risk of misclassification. This new framework has the potential to unclog the bottleneck of information extraction from massive digital data while ensuring a high level of accuracy in biodiversity assessment.

Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes.

Coral reefs host hundreds of thousands of animal species that are increasingly threatened by anthropogenic disturbances. These animals host microbial communities at their surface, playing crucial roles for their fitness. However, the diversity of such microbiomes is mostly described in a few coral species and still poorly defined in other invertebrates and vertebrates. Given the diversity of animal microbiomes, and the diversity of host species inhabiting coral reefs, the contribution of such microbiomes to the total microbial diversity of coral reefs could be important, yet potentially vulnerable to the loss of animal species. Analysis of the surface microbiome from 74 taxa, including teleost fishes, hard and soft corals, crustaceans, echinoderms, bivalves and sponges, revealed that more than 90% of their prokaryotic phylogenetic richness was specific and not recovered in surrounding plankton. Estimate of the total richness associated with coral reef animal surface microbiomes reached up to 2.5% of current estimates of Earth prokaryotic diversity. Therefore, coral reef animal surfaces should be recognized as a hotspot of marine microbial diversity. Loss of the most vulnerable reef animals expected under present-day scenarios of reef degradation would induce an erosion of 28% of the prokaryotic richness, with unknown consequences on coral reef ecosystem functioning.

Meeting fisheries, ecosystem function, and biodiversity goals in a human-dominated world.

The worldwide decline of coral reefs necessitates targeting management solutions that can sustain reefs and the livelihoods of the people who depend on them. However, little is known about the context in which different reef management tools can help to achieve multiple social and ecological goals. Because of nonlinearities in the likelihood of achieving combined fisheries, ecological function, and biodiversity goals along a gradient of human pressure, relatively small changes in the context in which management is implemented could have substantial impacts on whether these goals are likely to be met. Critically, management can provide substantial conservation benefits to most reefs for fisheries and ecological function, but not biodiversity goals, given their degraded state and the levels of human pressure they face.

Species diversity and composition drive the aesthetic value of coral reef fish assemblages.

Cultural and recreational values of biodiversity are considered as important dimensions of nature's contribution to people. Among these values, the aesthetics can be of major importance as the appreciation of beauty is one of the simplest forms of human emotional response. Using an online survey, we disentangled the effects of different facets of biodiversity on aesthetic preferences of coral reef fish assemblages that are among the most emblematic assemblages on Earth. While we found a positive saturating effect of species' richness on human preference, we found a net negative effect of species abundance, no effect of species functional diversity and contrasting effects of species composition depending on species' attractiveness. Our results suggest that the biodiversity-human interest relationship is more complex than has been previously stated. By integrating several scales of organization, our study is a step forward in better evaluating the aesthetic value of biodiversity.

Fish communities diverge in species but converge in traits over three decades of warming.

Describing the spatial and temporal dynamics of communities is essential for understanding the impacts of global environmental change on biodiversity and ecosystem functioning. Trait-based approaches can provide better insight than species-based (i.e. taxonomic) approaches into community assembly and ecosystem functioning, but comparing species and trait dynamics may reveal important patterns for understanding community responses to environmental change. Here, we used a 33-year database of fish monitoring to compare the spatio-temporal dynamics of taxonomic and trait structure in North Sea fish communities. We found that the majority of variation in both taxonomic and trait structure was explained by a pronounced spatial gradient, with distinct communities in the southern and northern North Sea related to depth, sea surface temperature, salinity and bed shear stress. Both taxonomic and trait structure changed significantly over time; however taxonomically, communities in the south and north diverged towards different species, becoming more dissimilar over time, yet they converged towards the same traits regardless of species differences. In particular, communities shifted towards smaller, faster growing species with higher thermal preferences and pelagic water column position. Although taxonomic structure changed over time, its spatial distribution remained relatively stable, whereas in trait structure, the southern zone of the North Sea shifted northward and expanded, leading to homogenization. Our findings suggest that global environmental change, notably climate warming, will lead to convergence towards traits more adapted for novel environments regardless of species composition.