Aim Mesophotic coral ecosystems (MCEs) are unique communities that support a high proportion of depth‐endemic species distinct from shallow‐water coral reefs. However, there is currently little consensus on the boundaries between shallow and mesophotic coral reefs and between upper versus lower MCEs because studies of these communities are often site specific. Here, we examine the ecological evidence for community breaks, defined here as species loss, in fish and benthic taxa between shallow reefs and MCEs globally. Location Global MCEs. Time period 1973–2017. Major taxa studied Macrophytes, Porifera, Scleractinia, Hydrozoa, Octocorallia, Antipatharia and teleost fishes. Methods We used random‐effects models and breakpoint analyses on presence/absence data to identify regions of higher than expected species loss along a depth gradient of 1–69 m, based on a meta‐analysis of 26 studies spanning diverse photoautotrophic and heterotrophic taxa. We then investigated the extent to which points of high faunal turnover can be explained by environmental factors, including light, temperature and nutrient availability. Results We found evidence for a community break, indicated by a significant loss of shallow‐water taxa, at ~ 60 m across several taxonomically and functionally diverse benthic groups and geographical regions. The breakpoint in benthic composition is best explained by decreasing light, which is correlated with the optical depths between 10 and 1% of surface irradiance. A concurrent shift in the availability of nutrients, both dissolved and particulate organic matter, and a shift from photoautotroph to heterotroph‐dominated assemblages also occurs at ~ 60 m depth. Main conclusions We found evidence for global community breaks across multiple benthic taxa at ~ 60 m depth, indicative of distinct community transitions between shallow and mesophotic coral ecosystems. Changes in the underwater light environment and the availability of trophic resources along the depth gradient are the most parsimonious explanations for the observed patterns.

Sponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge‐loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (< 30 m) cryptic species. However, support for this hypothesis at mesophotic depths (∼ 30–150 m) is lacking. Here, we examined detritus production, a prerequisite of the sponge loop pathway, in a reciprocal transplant experiment, using Halisarca caerulea from water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples of H. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes in Oxyphotobacteria, Acidimicrobiia, Nitrososphaeria, Nitrospira, Deltaproteobacteria, and Dadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

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Agelas tubulata from shallow to mesophotic depths on Grand Cayman Island.

Sponges are a crucial component of Caribbean coral reef ecosystem structure and function. In the Caribbean, many sponges show a predictable increase in percent cover or abundance as depth increases from shallow (< 30 m) to mesophotic (30–150 m) depths. Given that sponge abundances are predicted to increase in the Caribbean as coral cover declines, understanding ecological factors that control their distribution is critical. Here we assess if sponge cover increases as depth increases into the mesophotic zone for three common Caribbean reef sponges, Xestospongia muta, Agelas tubulata, and Plakortis angulospiculatus, and use stable isotope analyses to determine whether shifts in trophic resource utilization along a shallow to mesophotic gradient occurred. Ecological surveys show that all target sponges significantly increase in percent cover as depth increases. Using bulk stable isotope analysis, we show that as depth increases there are increases in the δ13C and δ15N values, reflecting that all sponges consumed more heterotrophic picoplankton, with low C:N ratios in the mesophotic zone. However, compound‐specific isotope analysis of amino acids (CSIA‐AA) shows that there are species‐specific increases in δ13CAA and δ15NAA values. Xestospongia muta and P. angulospiculatus showed a reduced reliance on photoautotrophic resources as depth increased, while A. tubulata appears to rely on heterotrophy at all depths. The δ13CAA and δ15NAA values of these sponges also reflect species‐specific patterns of host utilization of both POM and dissolved organic matter (DOM), its subsequent re‐synthesis, and translocation, by their microbiomes.

Studies on the trophic ecology of scleractinian corals often include stable isotope analyses of tissue and symbiont carbon and nitrogen. These approaches have provided critical insights into the trophic sources and sinks that are essential to understanding larger-scale carbon and nitrogen budgets on coral reefs. While stable isotopes have identified most shallow water (<30 m) corals as mixotrophic, with variable dependencies on autotrophic versus heterotrophic resources, corals in the mesophotic zone (~30–150 m) transition to heterotrophy with increasing depth because of decreased photosynthetic productivity. Recently, these interpretations of the stable isotope data to distinguish between autotrophy and heterotrophy have been criticized because they are confounded by increased nutrients, reverse translocation of photosynthate, and changes in irradiance that do not influence photosynthate translocation. Here we critically examine the studies that support these criticisms and show that they are contextually not relevant to interpreting the transition to heterotrophy in corals from shallow to mesophotic depths. Additionally, new data and a re-analysis of previously published data show that additional information (e.g., skeletal isotopic analysis) improves the interpretation of bulk stable isotope data in determining when a transition from primary dependence on autotrophy to heterotrophy occurs in scleractinian corals.

Black band is a deadly coral disease found worldwide, which may become more virulent as oceanic conditions continue to change. To determine the effects of climate change and ocean acidification on black band disease virulence, Orbicella faveolata corals with black band were exposed to different temperature and pH conditions. Results showed a significant decrease in disease progression under low pH (7.7) conditions. Low pH also altered the relative abundance of the bacterial community of the black band disease consortium. Here, there was a significant decrease in Roseofilum, the cyanobacterium that typically dominates the black band mat. These results indicate that as oceanic pH decreases so may the virulence of a worldwide coral disease.

Sponges are increasingly recognized as an ecologically important taxon on coral reefs, representing significant biomass and biodiversity where sponges have replaced scleractinian corals. Most sponge species can be divided into two symbiotic states based on symbiont community structure and abundance (i.e., the microbiome), and are characterized as high microbial abundance (HMA) or low microbial abundance (LMA) sponges. Across the Caribbean, sponge species of the HMA or LMA symbiotic states differ in metabolic capacity, as well as their trophic ecology. A metagenetic analysis of symbiont 16 S rRNA and metagenomes showed that HMA sponge microbiomes are more functionally diverse than LMA microbiomes, offer greater metabolic functional capacity and redundancy, and encode for the biosynthesis of secondary metabolites. Stable isotope analyses showed that HMA and LMA sponges primarily consume dissolved organic matter (DOM) derived from external autotrophic sources, or live particulate organic matter (POM) in the form of bacterioplankton, respectively, resulting in a low degree of resource competition between these symbiont states. As many coral reefs have undergone phase shifts from coral- to macroalgal-dominated reefs, the role of DOM, and the potential for future declines in POM due to decreased picoplankton productivity, may result in an increased abundance of chemically defended HMA sponges on tropical coral reefs.