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1. Trophic ecology of Caribbean sponges in the mesophotic zone

   https://doi.org/10.1002/lno.11668  

   Macartney, Keir J. ; Slattery, Marc ; Lesser, Michael P. ( December 2020 , Limnology and Oceanography)

   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, andPlakortis 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 δ¹³C_AAand δ¹⁵N_AAvalues.Xestospongia mutaandP. angulospiculatusshowed a reduced reliance on photoautotrophic resources as depth increased, whileA. tubulataappears to rely on heterotrophy at all depths. The δ¹³C_AAand δ¹⁵N_AAvalues 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.

    

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2. Depth‐dependent detritus production in the sponge, Halisarca caerulea

   https://doi.org/10.1002/lno.11384  

   Lesser, Michael P. ; Mueller, Benjamin ; Pankey, M. Sabrina ; Macartney, Keir J. ; Slattery, Marc ; de Goeij, Jasper M. ( December 2019 , Limnology and Oceanography)

   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, usingHalisarca caeruleafrom water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples ofH. 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 inOxyphotobacteria,Acidimicrobiia,Nitrososphaeria,Nitrospira,Deltaproteobacteria, andDadabacteriia. 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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3. Global community breaks at 60 m on mesophotic coral reefs

   https://doi.org/10.1111/geb.12940  

   Lesser, Michael P. ; Slattery, Marc ; Laverick, Jack H. ; Macartney, Keir J. ; Bridge, Tom C. ; Pandolfi, ed., John ( June 2019 , Global Ecology and Biogeography)

   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.

   Global MCEs.

   1973–2017.

   Macrophytes, Porifera, Scleractinia, Hydrozoa, Octocorallia, Antipatharia and teleost fishes.

   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.

   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.

   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.

    

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4. Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

   https://doi.org/10.1038/s43705-022-00196-3  

   Lesser, Michael P. ; Pankey, M. Sabrina ; Slattery, Marc ; Macartney, Keir J. ; Gochfeld, Deborah J. ( November 2022 , ISME Communications)

   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.

    

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5. Production of phytodetritus by a coral reef sponge increases from shallow to mesophotic depths

   https://doi.org/10.1002/lno.12342  

   Lesser, Michael P. ; Macartney, Keir J. ; Slattery, Marc ( April 2023 , Limnology and Oceanography)

   On Caribbean coral reefs, sponges are important members of the benthic community and have an important role in consuming particulate organic matter (POM) and dissolved organic matter (DOM), with the subsequent production of detritus that is then shunted into a process now referred to as the “sponge‐loop.” An emergent species of sponge commonly found on Caribbean coral reefs,Agelas tubulata, increases in size and growth rate from shallow (< 30 m) to mesophotic depths (30–150 m) on Grand Cayman Island.A.tubulatadepends largely on heterotrophy across shallow to mesophotic depths and has been shown to utilize detritus on shallow reefs. However, detritus production byA.tubulataon shallow and mesophotic coral reefs has not been previously reported. Here we show, using flow cytometry, that sponge detritus includes a previously unquantified component, phytodetritus. Sponge phytodetritus production was shown experimentally to be greater in sponges from mesophotic depths compared to sponges from shallow coral reefs. Additionally, the size range of this phytodetritus corresponds to the size range of autotrophic picoplankton, primarily prochlorophytes, known to be an important food source for filter‐feeding sponges. Given the known lability of phytodetritus, compared to other more recalcitrant components of the detrital pool, its role in the food web of mesophotic communities combined with the increased availability of live POM, may be an underappreciated component of mesophotic community carbon and nitrogen flow.

    

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