Host diet drives gut microbiome convergence between coral reef fishes and mammals.

Animal gut microbiomes are critical to host physiology and fitness. The gut microbiomes of fishes-the most abundant and diverse vertebrate clade-have received little attention relative to other clades. Coral reef fishes, in particular, make up a wide range of evolutionary histories and feeding ecologies that are likely associated with gut microbiome diversity. The repeated evolution of herbivory in fishes and mammals also allows us to examine microbiome similarity in relationship to diet across the entire vertebrate tree of life. Here, we generate a large coral reef fish gut microbiome dataset (n = 499 samples, 19 species) and combine it with a diverse aggregation of public microbiome data (n = 447) to show that host diet drives significant convergence between coral reef fish and mammalian gut microbiomes. We demonstrate that this similarity is largely driven by carnivory and herbivory and that herbivorous and carnivorous hosts exhibit distinct microbial compositions across fish and mammals. We also show that fish and mammal gut microbiomes share prominent microbial taxa, including Ruminoccocus spp. and Akkermansia spp., and predicted metabolic pathways. Despite the major evolutionary and ecological differences between fishes and mammals, our results reveal that their gut microbiomes undergo similar dietary selective pressures. Thus, diet, in addition to phylosymbiosis must be considered even when comparing the gut microbiomes of distantly related hosts.

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.

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.

Paternal care regulates the timing, synchrony and success of hatching in a coral reef fish.

In oviparous species, the timing of hatching is a crucial decision, but for developing embryos, assessing cues that indicate the optimal time to hatch is challenging. In species with pre-hatching parental care, parents can assess environmental conditions and induce their offspring to hatch. We provide the first documentation of parental hatching regulation in a coral reef fish, demonstrating that male neon gobies (Elacatinus colini) directly regulate hatching by removing embryos from the clutch and spitting hatchlings into the water column. All male gobies synchronized hatching within 2 h of sunrise, regardless of when eggs were laid. Paternally incubated embryos hatched later in development, more synchronously, and had higher hatching success than artificially incubated embryos that were shaken to provide a vibrational stimulus or not stimulated. Artificially incubated embryos displayed substantial plasticity in hatching times (range: 80-224 h post-fertilization), suggesting that males could respond to environmental heterogeneity by modifying the hatching time of their offspring. Finally, paternally incubated embryos hatched with smaller yolk sacs and larger propulsive areas than artificially incubated embryos, suggesting that paternal effects on hatchling phenotypes may influence larval dispersal and fitness. These findings highlight the complexity of fish parental care behaviour and may have important, and currently unstudied, consequences for fish population dynamics.

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.

Functional niches of cleanerfish species are mediated by habitat use, cleaning intensity and client selectivity.

An animal's functional niche is a complex, multidimensional construct, mediated by an individual's morphology, physiology and behaviour. Behavioural aspects of the niche can be difficult to quantify, as their expression is often subtle and tailored to an infinite number of different situations that involve sophisticated mechanisms such as mutualisms, species dominance or fear effects. The extreme diversity of tropical fish assemblages has led to extensive debate over the extent to which species differ in their resource use and functional role. Ectoparasite removal by cleanerfish species is considered a behaviourally complex interspecific interaction in vertebrates, but differences in the services rendered by various species of cleanerfish, and potential consequences for the range of clients (i.e. resources) they attract, have rarely been examined. Here, we quantify differences among three coexisting species of morphologically similar cleaner wrasses (Labroides bicolor, L. dimidiatus and L. pectoralis) in the global centre of marine biodiversity, the Coral Triangle. We found no clear taxonomic partitioning of clients among cleanerfishes. However, the three cleanerfish species exhibited distinct habitat preferences, and differed in their cleaning intensity: L. bicolor serviced the fewest species and clients, while L. pectoralis serviced the most clients and spent the most time cleaning. Accordingly, L. pectoralis showed no preference for clients based on client size or abundance, while both L. bicolor and L. dimidiatus had a higher likelihood of interacting with clients based on their size (larger client species in L. bicolor, smaller client species in L. dimidiatus) and abundance (more abundant client species for both). Our results suggest that the services rendered by the three species of cleanerfishes differ in their spatial availability, quality and selectivity, thus permitting the coexistence of these species despite their ecological similarity. This, in turn, creates a complex seascape of species-specific cleaning services that underpins crucial biotic interactions in the ocean's most diverse ecosystem.

Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes.

Ectotherms exhibit considerable plasticity in their life-history traits. This plasticity can reflect variability in environmental and social factors, but the causes of observed patterns are often obscured with increasing spatial scales. We surveyed dichromatic parrotfishes across the northern Great Barrier Reef to examine variation in body size distributions and concomitant size at sex change (L∆50 ) against hypotheses of directional influence from biotic and abiotic factors known to affect demography. By integrating top-down, horizontal, and bottom-up processes, we demonstrate a strong association between exposure regimes (which are known to influence nutritional ecology and mating systems) and both body size distribution and L∆50 (median length at female-to-male sex change), with an accompanying lack of strong empirical support for other biotic drivers previously hypothesized to affect body size distributions. Across sites, body size was predictably linked to variation in temperature and productivity, but the strongest predictor was whether subpopulations occurred at sheltered mid and inner shelf reefs or at wave-exposed outer shelf reef systems. Upon accounting for the underlying influence of body size distribution, this habitat-exposure gradient was highly associated with further L∆50 variation across species, demonstrating that differences in mating systems across exposure gradients affect the timing of sex change beyond variation concomitant with differing overall body sizes. We posit that exposure-driven differences in habitat disturbance regimes have marked effects on the nutritional ecology of parrotfishes, leading to size-related variation in mating systems, which underpin the observed patterns. Our results call for better integration of life-history, social factors, and ecosystem processes to foster an improved understanding of complex ecosystems such as coral reefs.

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.

Microtopographic refuges shape consumer-producer dynamics by mediating consumer functional diversity.

Consumer-producer dynamics are critical for ecosystem functioning. In marine environments, primary production is often subject to strong consumer control, and on coral reefs, the grazing pressure exerted by herbivorous fishes has been identified as a major determinant of benthic community structure. Using experimental surfaces, we demonstrate that on coral reefs, microtopographic refuges decrease the overall grazing pressure by more than one order of magnitude. Furthermore, by functionally characterizing consumer communities, we show that refuges also restrict grazer communities to only one functional group, algal croppers, which selectively remove the apical parts of algae. In contrast, detritivorous fishes, which intensively graze flat and exposed microhabitats and can remove both particulate matter and entire stands of algal filaments, are almost entirely excluded. This preclusion of an entire ecosystem process (the removal of particulates) results in two distinct coexisting benthic regimes: communities within refuges are diverse and characterized by numerous algal types and juvenile scleractinian corals, while communities outside refuges support only low-diversity assemblages dominated by simple, unbranched filamentous turf algal mats. Although limited to the scale of a few centimeters, microtopographic refuges can, therefore, mediate the biotic control of community development by affecting both overall grazing rates and the functional diversity of consumer communities. We suggest that the coexistence of two distinct benthic regimes at a small spatial scale may be an important factor for ecosystem functioning and highlight the need to consider the ecological complexity of consumer-producer dynamics when assessing the status of coral reef ecosystems.

Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use.

Patterns of ecological specialization offer invaluable information about ecosystems. Yet, specialization is rarely quantified across several ecological niche axes and variables beyond the link between morphological and dietary specialization have received little attention. Here, we provide a quantitative evaluation of ecological specialization in a coral reef fish assemblage (f. Acanthuridae) along one fundamental and two realized niche axes. Specifically, we examined ecological specialization in 10 surgeonfish species with regards to morphology and two realized niche axes associated with diet and foraging microhabitat utilization using a recently developed multidimensional framework. We then investigated the potential relationships between morphological and behavioural specialization. These relationships differed markedly from the traditional ecomorphological paradigm. While morphological specialization showed no relationship with dietary specialization, it exhibited a strong relationship with foraging microhabitat specialization. However, this relationship was inverted: species with specialized morphologies were microhabitat generalists, whereas generalized morphotypes were microhabitat specialists. Interestingly, this mirrors relationships found in plant-pollinator communities and may also be applicable to other ecosystems, highlighting the potential importance of including niche axes beyond dietary specialization into ecomorphological frameworks. On coral reefs, it appears that morphotypes commonly perceived as most generalized may, in fact, be specialized in exploiting flat and easily accessible microhabitats.