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How coral reefs survive as oases of life in low-productivity oceans has puzzled scientists for centuries. The answer may lie in internal nutrient cycling and/or input from the pelagic zone. Integrating meta-analysis, field data, and population modeling, we show that the ocean’s smallest vertebrates, cryptobenthic reef fishes, promote internal reef fish biomass production through extensive larval supply from the pelagic environment. Specifically, cryptobenthics account for two-thirds of reef fish larvae in the near-reef pelagic zone despite limited adult reproductive outputs. This overwhelming abundance of cryptobenthic larvae fuels reef trophodynamics via rapid growth and extreme mortality, producing almost 60% of consumed reef fish biomass. Although cryptobenthics are often overlooked, their distinctive demographic dynamics may make them a cornerstone of ecosystem functioning on modern coral reefs.

Understanding species’ roles in food webs requires an accurate assessment of their trophic niche. However, it is challenging to delineate potential trophic interactions across an ecosystem, and a paucity of empirical information often leads to inconsistent definitions of trophic guilds based on expert opinion, especially when applied to hyperdiverse ecosystems. Using coral reef fishes as a model group, we show that experts disagree on the assignment of broad trophic guilds for more than 20% of species, which hampers comparability across studies. Here, we propose a quantitative, unbiased, and reproducible approach to define trophic guilds and apply recent advances in machine learning to predict probabilities of pairwise trophic interactions with high accuracy. We synthesize data from community-wide gut content analyses of tropical coral reef fishes worldwide, resulting in diet information from 13,961 individuals belonging to 615 reef fish. We then use network analysis to identify 8 trophic guilds and Bayesian phylogenetic modeling to show that trophic guilds can be predicted based on phylogeny and maximum body size. Finally, we use machine learning to test whether pairwise trophic interactions can be predicted with accuracy. Our models achieved a misclassification error of less than 5%, indicating that our approach results in a quantitative and reproducible trophic categorization scheme, as well as high-resolution probabilities of trophic interactions. By applying our framework to the most diverse vertebrate consumer group, we show that it can be applied to other organismal groups to advance reproducibility in trait-based ecology. Our work thus provides a viable approach to account for the complexity of predator–prey interactions in highly diverse ecosystems.

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. The relative importance of evolutionary history and ecology for traits that drive ecosystem processes is poorly understood. Analyzing nine traits associated with fish stoichiometry from 1,572 individuals yields multiple lines of evidence that phylogeny is a critical determinant of nutrient cycling in coral reefs.

Fish fecundity scales hyperallometrically with body mass, meaning larger females produce disproportionately more eggs than smaller ones. We explore this relationship beyond the species-level to estimate the “reproductive potential” of 1633 coral reef sites distributed globally. We find that, at the site-level, reproductive potential scales hyperallometrically with assemblage biomass, but with a smaller median exponent than at the species-level. Across all families, modelled reproductive potential is greater in fully protected sites versus fished sites. This difference is most pronounced for the important fisheries family, Serranidae. When comparing a scenario where 30% of sites are randomly fully protected to a current protection scenario, we estimate an increase in the reproductive potential of all families, and particularly for Serranidae. Such results point to the possible ecological benefits of the 30 × 30 global conservation target and showcase management options to promote the sustainability of population replenishment. This study estimates the reproductive potential of fish in globally distributed coral reef sites. The results show substantial gains in reproductive potential can be achieved through the 30 × 30 conservation target, particularly for the important fisheries family, Serranidae, demonstrating the possible benefit of protection to population replenishment.

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. Intestinal morphology is key to integrating digestive and assimilative processes into trait‐based approaches. Yet intestinal length alone has been commonly use for this purpose in fishes. Our study demonstrates that evolution and ecology have shaped a great diversity of intestinal morphologies in coral reef fishes that cannot be captured by length alone. We show that intestinal traits are clear indicators of fish trophic roles and intestinal surface area may be a most suitable trait to apply in functional studies than intestinal length.

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 [AMRfield]). 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 AMRfield and SMR) varies from 1.2 to 3.2 across species and body sizes. Furthermore, we illustrate that the scaling exponent for AMRfield varies across species and can substantially exceed the widely assumed value of 0.75 for SMR. Finally, by scaling organismal AMRfield 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. We know little about the metabolic demand of fishes in the wild. We propose a new approach to estimate active field metabolic rates by combining laboratory‐based respirometry and field‐based stereo‐video systems.

DNA metabarcoding is an increasingly popular technique to investigate biodiversity; however, many methodological unknowns remain, especially concerning the biases resulting from marker choice. Regions of the cytochrome c oxidase subunit I (COI) and 18S rDNA (18S) genes are commonly employed “universal” markers for eukaryotes, but the extent of taxonomic biases introduced by these markers and how such biases may impact metabarcoding performance is not well quantified. Here, focusing on macroeukaryotes, we use standardized sampling from autonomous reef monitoring structures (ARMS) deployed in the world's most biodiverse marine ecosystem, the Coral Triangle, to compare the performance of COI and 18S markers. We then compared metabarcoding data to image‐based annotations of ARMS plates. Although both markers provided similar estimates of taxonomic richness and total sequence reads, marker choice skewed estimates of eukaryotic diversity. The COI marker recovered relative abundances of the dominant sessile phyla consistent with image annotations. Both COI and the image annotations provided higher relative abundance estimates of Bryozoa and Porifera and lower estimates of Chordata as compared to 18S, but 18S recovered 25% more phyla than COI. Thus, while COI more reliably reflects the occurrence of dominant sessile phyla, 18S provides a more holistic representation of overall taxonomic diversity. Ideal marker choice is, therefore, contingent on study system and research question, especially in relation to desired taxonomic resolution, and a multimarker approach provides the greatest application across a broad range of research objectives. As metabarcoding becomes an essential tool to monitor biodiversity in our changing world, it is critical to evaluate biases associated with marker choice. We used standardized sampling from autonomous reef monitoring structures (ARMS) deployed in the world's most biodiverse marine ecosystem, the Coral Triangle, to compare the performance of COI and 18S markers, as well as comparing metabarcoding data to image‐based annotations of ARMS plates. Although both markers provided similar estimates of taxonomic richness and total sequence reads, marker choice skewed estimates of eukaryotic diversity: while COI more reliably reflects the occurrence of dominant sessile phyla, 18S provides a more holistic representation of overall taxonomic diversity. Ideal marker choice is, therefore, contingent on study system and research question, and a multimarker approach provides the greatest application across a broad range of research objectives.

Remote underwater video (RUV) surveys are increasingly replacing diver‐based underwater visual censuses (UVCs) in fish ecology studies, especially on coral reefs. However, extracting reliable estimates of abundance or density from video footage is a major challenge, with most studies using a metric of relative abundance, MaxN (maximum number of concurrent conspecific individuals). Here we compare a video survey density estimation method used in terrestrial wildlife management, random encounter staying time modelling (REST) to MaxN from unbaited videos and density estimates from diver‐based UVC. We assess and compare the three approaches according to labour intensiveness (survey time effort per m2), species detection, abundance estimates and potential biases against size or aggregation behaviour. We found that species detection in REST was highly sensitive to sampling effort due to the minimum number of detections required for model fitting. There was also considerable variation in REST‐estimated absolute densities between species compared with other methods, however, each method was able to detect compositional differences among sites. While UVC was far less labour intensive than REST or MaxN in survey and processing effort, species richness was consistently lower in UVC observations compared to that from the two video‐based approaches. Pairwise generalised linear mixed models between method abundances showed that UVC abundances tended to be higher than other methods for shoaling/schooling fish. Our study identified strengths and weaknesses in each method for specific research objectives that may prioritise species detections or precision in abundance estimates. Although labour intensive, we found REST a viable alternative to MaxN if absolute abundance estimates are preferred. If precise abundance estimates are not a priority and labour is limited, we found MaxN suitable for capturing species richness. Finally, UVC ranked best in labour effectiveness in terms of both person‐hours and spatial coverage, and it provided good estimates of abundance, but generally lower species richness. Ultimately, method selection depends on study‐specific priorities and trade‐offs.

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. Integrating bioenergetic models and global coral reef fish community surveys, the authors show that there are functional trade-offs, meaning that no community can maximize all functions, and that dominant species underpin local functions, but their identity varies geographically.

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. Measurement(s) growth Technology Type(s) otolithometry Sample Characteristic - Organism Actinopterygii Sample Characteristic - Environment coral reef Sample Characteristic - Location French Polynesia Machine-accessible metadata file describing the reported data: https://doi.org/10.6084/m9.figshare.13027817