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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.

Tropical ectotherms are hypothesized to be vulnerable to environmental changes, but cascading effects of organismal tolerances on the assembly and functioning of reef fish communities are largely unknown. Here, we examine differences in organismal traits, assemblage structure, and productivity of cryptobenthic reef fishes between the world’s hottest, most extreme coral reefs in the southern Arabian Gulf and the nearby, but more environmentally benign, Gulf of Oman. We show that assemblages in the Arabian Gulf are half as diverse and less than 25% as abundant as in the Gulf of Oman, despite comparable benthic composition and live coral cover. This pattern appears to be driven by energetic deficiencies caused by responses to environmental extremes and distinct prey resource availability rather than absolute thermal tolerances. As a consequence, production, transfer, and replenishment of biomass through cryptobenthic fish assemblages is greatly reduced on Earth’s hottest coral reefs. Extreme environmental conditions, as predicted for the end of the 21st century, could thus disrupt the community structure and productivity of a critical functional group, independent of live coral loss. Brandl, Johansen et al. compare organismal traits, community structure, and productivity dynamics of cryptobenthic reef fishes across two locations, the Arabian Gulf and the Gulf of Oman, the former of which harbors the world’s hottest coral reefs. They show that environmental extremes in the Arabian Gulf result in dramatically less diverse, abundant, and productive cryptobenthic fish assemblages, which could foreshadow the future of coral reef biodiversity and functioning.

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.

By cultivating turf algae and aggressively defending their territories, territorial damselfishes in the genus Stegastes play a major role in shaping coral-algal dynamics on coral reefs. The epilithic algal matrix (EAM) inside Stegastes ’ territories is known to harbor high abundances of potential coral disease pathogens. To determine the impact of territorial grazers on coral microbial assemblages, we established a coral transplant inside and outside of Stegastes ’ territories. Over the course of one year, the percent mortality of transplanted corals was monitored and coral samples were collected for microbial analysis. As compared to outside damselfish territories, Stegastes were associated with a higher rate of mortality of transplanted corals. However, 16S rDNA sequencing revealed that territorial grazers do not differentially impact the microbial assemblage of corals exposed to the EAM. Regardless of Stegastes presence or absence, coral transplantation resulted in a shift in the coral-associated microbial community and an increase in coral disease associated potential pathogens. Further, transplanted corals that suffer low to high mortality undergo a microbial transition from a microbiome similar to that of healthy corals to that resembling the EAM. These findings demonstrate that coral transplantation significantly impacts coral microbial communities and transplantation may increase susceptibility to coral disease.

Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world’s landscapes and biodiversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish ( Stegastes diencaeus ) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps ( Mysidium integrum ). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domestication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved. It has been hypothesized that domestication can occur through the ‘commensal pathway’ in which the domesticate takes advantage of a niche created as a byproduct by the domesticator. Here, Brooker et al. provide evidence for a commensal domestication process between longfin damselfish and mysid shrimps.

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.

Climate change is the greatest threat to coral reef ecosystems. Importantly, gradual changes in seawater chemistry compounds upon increasing temperatures leading to declines in calcification and survivorship of reef-building corals. To assess relative versus synergistic effects of warming versus ocean acidification, Acropora muricata and Acropora hyacinthus were subjected to three temperature treatments (26 °C, 28.5 °C, 31 °C) crossed with three levels of pCO2 (410 μatm, 652 μatm, 934 μatm), representing current, mid and end-of-century scenarios for 12 weeks. Temperature increased gradually in the tanks from 26 °C to target temperatures over 5 weeks. Once stress was evident in the 31 °C (+ 2.5 °C above historical summer max) tanks, water temperature was decreased to normal summertime levels (29 °C) to assess recovery. pCO2 was gradually changed from control values (410 μatm) to target values over a 3 week period where they remained constant until the end of the experiment at 12 weeks. Temperature stress (31 °C) significantly impacted survivorship (90–95% decline), and over the long-term, there was a 50–90% decline in calcification across both coral species. Negative effects of mid and end-of-century pCO2 were largely independent of temperature and caused moderate reductions (36–74%) in calcification rates compared to temperature, over the long-term. Corals that survived temperature stress had higher lipid and protein content, showing that enhanced physiological condition provides an increased capacity to tolerate adverse temperatures. This study demonstrates that given the mortality rates in response to + 2.5 °C temperature stress, warming oceans (as opposed to ocean acidification) throughout the remainder of this century poses the greatest threat to reef-building corals.

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.

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. Our paper provides information concerning 3 metabolic rates (i.e., photosynthesis, respiration, and respiration) of 6 prominent coral reef taxas from Mo'orea. Moreover, we show that defining these 3 functions might explain coral reef dynamics after perturbations.

Biodiversity inventories and monitoring techniques for marine fishes often overlook small (<5 cm), bottom‐associated (‘cryptobenthic’) fishes, and few standardized, comparative assessments of cryptobenthic fish communities exist. We sought to develop a standardized, quantitative survey method for cryptobenthic fishes that permits their sampling across a variety of habitats and conditions. Fish‐specific autonomous reef monitoring structures (FARMS) are designed to sample cryptobenthic fishes using a suite of accessible and affordable materials. To generate a variety of microhabitats, FARMS consist of three layers of stacked PVC pipes in three different sizes, as well as a bottom and top level of loose PVC‐pipe fragments in a mesh basket. We deployed FARMS across a variety of habitats, including coral reefs, seagrass beds, oyster reefs, mangroves, and soft‐bottom habitats across six locations (Hawai'i, Texas, Panama, Saudi Arabia, Brazil, and Curaçao). From shallow estuaries to coral reefs beyond 100 m depth, FARMS attracted distinct communities of native cryptobenthic fishes with strong site or habitat specificity. Comparing the FARMS to communities sampled with alternative methods (enclosed clove‐oil stations on coral reefs in Panama and oyster sampling units on oyster reefs in Texas) suggests that FARMS yield a subset of cryptobenthic fish species that are representative of those present on local coral and oyster reefs. While FARMS yield fewer individuals per sample, they are efficient sampling devices relative to the sampled area. We demonstrate that FARMS represent a useful tool for standardized collections of cryptobenthic fishes. While natural substrata are bound to yield more mature communities with a larger number of individuals and wider range of specialist species, the potential to deploy and retrieve FARMS in turbid environments, beyond regular SCUBA depth, and where fish collections using anaesthetics or ichthyocides are forbidden suggests that they are a valuable complementary technique to survey fishes in aquatic ecosystems. Deploying FARMS in locations and habitats where cryptobenthic fish communities have not been studied in detail may yield many valuable specimens of unknown or poorly known species.