Fish feces reveal diverse nutrient sources for coral reefs.

Consumers mediate nutrient cycling through excretion and egestion across most ecosystems. In nutrient-poor tropical waters such as coral reefs, nutrient cycling is critical for maintaining productivity. While the cycling of fish-derived inorganic nutrients via excretion has been extensively investigated, the role of egestion for nutrient cycling has remained poorly explored. We sampled the fecal contents of 570 individual fishes across 40 species, representing six dominant trophic guilds of coral reef fishes in Moorea, French Polynesia. We measured fecal macro- (proteins, carbohydrates, lipids) and micro- (calcium, copper, iron, magnesium, manganese, zinc) nutrients and compared the fecal nutrient quantity and quality across trophic guilds, taxa, and body size. Macro- and micronutrient concentrations in fish feces varied markedly across species. Genera and trophic guild best predicted fecal nutrient concentrations. In addition, nutrient composition in feces was unique among species within both trophic guilds (herbivores and corallivores) and genera (Acanthurus and Chaetodon). Particularly, certain coral reef fishes (e.g., Thalassoma hardwicke, Chromis xanthura, Chaetodon pelewensis and Acanthurus pyroferus) harbored relatively high concentrations of micronutrients (e.g., Mn, Mg, Zn and Fe, respectively) that are known to contribute to ocean productivity and positively impact coral physiological performances. Given the nutrient-rich profiles across reef fish feces, conserving holistic reef fish communities ensures the availability of nutritional pools on coral reefs. We therefore suggest that better integration of consumer egestion dynamics into food web models and ecosystem-scale processes will facilitate an improved understanding of coral reef functioning.

Intestinal Microbiome Richness of Coral Reef Damselfishes (Actinopterygii: Pomacentridae).

Fish gastro-intestinal system harbors diverse microbiomes that affect the host's digestion, nutrition, and immunity. Despite the great taxonomic diversity of fish, little is understood about fish microbiome and the factors that determine its structure and composition. Damselfish are important coral reef species that play pivotal roles in determining algae and coral population structures of reefs. Broadly, damselfish belong to either of two trophic guilds based on whether they are planktivorous or algae-farming. In this study, we used 16S rRNA gene sequencing to investigate the intestinal microbiome of 5 planktivorous and 5 algae-farming damselfish species (Pomacentridae) from the Great Barrier Reef. We detected Gammaproteobacteria ASVs belonging to the genus Actinobacillus in 80% of sampled individuals across the 2 trophic guilds, thus, bacteria in this genus can be considered possible core members of pomacentrid microbiomes. Algae-farming damselfish had greater bacterial alpha-diversity, a more diverse core microbiome and shared 35 ± 22 ASVs, whereas planktivorous species shared 7 ± 3 ASVs. Our data also highlight differences in microbiomes associated with both trophic guilds. For instance, algae-farming damselfish were enriched in Pasteurellaceae, whilst planktivorous damselfish in Vibrionaceae. Finally, we show shifts in bacterial community composition along the intestines. ASVs associated with the classes Bacteroidia, Clostridia, and Mollicutes bacteria were predominant in the anterior intestinal regions while Gammaproteobacteria abundance was higher in the stomach. Our results suggest that the richness of the intestinal bacterial communities of damselfish reflects host species diet and trophic guild.

O sistema gastro-intestinal de peixes abriga microbiomas diversos que afetam a digestão, nutrição e imunidade do hospedeiro. Apesar da grande diversidade taxonômica dos peixes, entende-se pouco sobre o microbioma dos peixes e fatores que determinam sua estrutura e composição. Peixes-donzela são espécies importantes em recifes de coral que exercem papéis pivotais na determinação da estrutura de algas e corais dos recifes. De forma geral, peixes-donzela pertencem à uma de duas guildas tróficas dependendo se são planctívoros ou algívoros. Nesse estudo, usamos sequenciamento do gene 16S rRNA para investigar o microbioma intestinal de cinco espécies planctívoras e cinco espécies algívoras de peixes-donzela (Pomacentridae) da Grande Barreira de Corais. Detectamos ASVs de Gammaproteobacteria pertencendo ao gênero Actinobacillus em 80% dos indivíduos amostrados nas duas guildas tróficas, logo, bactérias desse gênero podem ser consideradas como possíveis membros essenciais do microbioma dos pomacentrídeos. Peixes-donzela algívoros apresentaram uma maior alpha-diversidade bacteriana, um microbioma essencial mais diverso e compartilharam 35 ± 22 ASVs, e espécies planctívoras compartilharam 7 ± 3 ASVs. Nossos dados também ilustram diferenças nos microbiomas associados com ambas guildas tróficas. Por exemplo, peixes-donzela algívoros estavam enriquecidos em Pasteurellaceae, enquanto peixes-donzela planctívoros, em Vibrionaceae. Finalmente, demonstramos mudanças na composição da comunidade bacteriana associada com as classes Bacteroidia, Clostridia e Mollicutes foram predominantes nas regiões intestinais anteriores enquanto a abundância de Gammaproteobacteria foi maior no estômago. Nossos resultados sugerem que a riqueza das comunidades bacterianas intestinais de peixes-donzela refletem a dieta da espécie do hospedeiro, bem como a sua guilda trófica.

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.

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.

Congruent trophic pathways underpin global coral reef food webs.

Ecological interactions uphold ecosystem structure and functioning. However, as species richness increases, the number of possible interactions rises exponentially. More than 6,000 species of coral reef fishes exist across the world's tropical oceans, resulting in an almost innumerable array of possible trophic interactions. Distilling general patterns in these interactions across different bioregions stands to improve our understanding of the processes that govern coral reef functioning. Here, we show that across bioregions, tropical coral reef food webs exhibit a remarkable congruence in their trophic interactions. Specifically, by compiling and investigating the structure of six coral reef food webs across distinct bioregions, we show that when accounting for consumer size and resource availability, these food webs share more trophic interactions than expected by chance. In addition, coral reef food webs are dominated by dietary specialists, which makes trophic pathways vulnerable to biodiversity loss. Prey partitioning among these specialists is geographically consistent, and this pattern intensifies when weak interactions are disregarded. Our results suggest that energy flows through coral reef communities along broadly comparable trophic pathways. Yet, these critical pathways are maintained by species with narrow, specialized diets, which threatens the existence of coral reef functioning in the face of biodiversity loss.

Nutrient pollution alters the gut microbiome of a territorial reef fish.

Human-induced nutrient pollution threatens coral reefs worldwide. Although eutrophication disrupts coral microbiomes, often leading to coral mortality, it is unknown whether eutrophication impacts the microbiomes of other coral reef organisms. Of particular interest are herbivorous fishes, whose algae consumption is critical in maintaining healthy corals. To examine the effects of eutrophication on fish gut microbiomes, we experimentally enriched territories of Stegastes nigricans, a predominantly herbivorous damselfish that farms turf algae. Using 16S RNA sequencing, we demonstrate that hindgut and foregut microbiomes have significantly higher alpha diversity in nutrient-enriched territories as compared to unenriched controls. S. nigricans gut microbiomes also exhibited significantly different compositions across treatments. In contrast, these changes were not observed in the microbiomes of the turf algae consumed by S. nigricans, indicating that the gut microbiome changes were autochthonous. Combined, our results provide a novel example of endogenous microbial shifts in wild vertebrates caused by simulated anthropogenic stress.

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.

Delineating reef fish trophic guilds with global gut content data synthesis and phylogeny.

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.

Domestication via the commensal pathway in a fish-invertebrate mutualism.

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.

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.

Extreme environmental conditions reduce coral reef fish biodiversity and productivity.

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.

Response to Comment on "Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning".

Allgeier and Cline suggest that our model overestimates the contributions of cryptobenthic fishes to coral reef functioning. However, their 20-year model ignores the basic biological limits of population growth. If incorporated, cryptobenthic contributions to consumed fish biomass remain high (20 to 70%). Disturbance cycles and uncertainties surrounding the fate of large fishes on decadal scales further demonstrate the important role of cryptobenthic fishes.

Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning.

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.

Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions.

Anthropogenic habitats are increasingly prevalent in coastal marine environments. Previous research on sessile epifauna suggests that artificial habitats act as a refuge for nonindigenous species, which results in highly homogenous communities across locations. However, vertebrate assemblages that live in association with artificial habitats are poorly understood. Here, we quantify the biodiversity of small, cryptic (henceforth "cryptobenthic") fishes from marine dock pilings across six locations over 35° of latitude from Maine to Panama. We also compare assemblages from dock pilings to natural habitats in the two southernmost locations (Panama and Belize). Our results suggest that the biodiversity patterns of cryptobenthic fishes from dock pilings follow a Latitudinal Diversity Gradient (LDG), with average local and regional diversity declining sharply with increasing latitude. Furthermore, a strong correlation between community composition and spatial distance suggests distinct regional assemblages of cryptobenthic fishes. Cryptobenthic fish assemblages from dock pilings in Belize and Panama were less diverse and had lower densities than nearby reef habitats. However, dock pilings harbored almost exclusively native species, including two species of conservation concern absent from nearby natural habitats. Our results suggest that, in contrast to sessile epifaunal assemblages on artificial substrates, artificial marine habitats can harbor diverse, regionally characteristic assemblages of vertebrates that follow macroecological patterns that are well documented for natural habitats. We therefore posit that, although dock pilings cannot function as a replacement for natural habitats, dock pilings may provide cost-effective means to preserve native vertebrate biodiversity, and provide a habitat that can be relatively easily monitored to track the status and trends of fish biodiversity in highly urbanized coastal marine environments.

A test of trophic cascade theory: fish and benthic assemblages across a predator density gradient on coral reefs.

Removal of predators is often hypothesized to alter community structure through trophic cascades. However, despite recent advances in our understanding of trophic cascades, evidence is often circumstantial on coral reefs because fishing pressure frequently co-varies with other anthropogenic effects, such as fishing for herbivorous fishes and changes in water quality due to pollution. Australia's outer Great Barrier Reef (GBR) has experienced fishing-induced declines of apex predators and mesopredators, but pollution and targeting of herbivorous fishes are minimal. Here, we quantify fish and benthic assemblages across a fishing-induced predator density gradient on the outer GBR, including apex predators and mesopredators to herbivores and benthic assemblages, to test for evidence of trophic cascades and alternative hypotheses to trophic cascade theory. Using structural equation models, we found no cascading effects from apex predators to lower trophic levels: a loss of apex predators did not lead to higher levels of mesopredators, and this did not suppress mobile herbivores and drive algal proliferation. Likewise, we found no effects of mesopredators on lower trophic levels: a decline of mesopredators was not associated with higher abundances of algae-farming damselfishes and algae-dominated reefs. These findings indicate that top-down forces on coral reefs are weak, at least on the outer GBR. We conclude that predator-mediated trophic cascades are probably the exception rather than the rule in complex ecosystems such as the outer GBR.

Coral transplantation triggers shift in microbiome and promotion of coral disease associated potential pathogens.

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.

Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease.

Microbial community structure on coral reefs is strongly influenced by coral-algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae), such as Stegastes, mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages and coral health, we determined the benthic community composition (epilithic algal matrix and prokaryotes) and coral disease prevalence inside and outside of damselfish territories in the Great Barrier Reef, Australia. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes's territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans's territories. These findings demonstrate the first link between fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease.