Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras.

Christopher J Freeman,Cole G Easson,David M Baker

doi:10.7717/peerj.695

Christopher J Freeman, Cole G Easson + Show 1 more

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https://doi.org/10.7717/peerj.695

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Abstract

Hosting symbionts provides many eukaryotes with access to the products of microbial metabolism that are crucial for host performance. On tropical coral reefs, many (High Microbial Abundance [HMA]) but not all (Low Microbial Abundance [LMA]) marine sponges host abundant symbiont communities. Although recent research has revealed substantial variation in these sponge-microbe associations (termed holobionts), little is known about the ecological implications of this diversity. We investigated the expansion of diverse sponge species across isotopic niche space by calculating niche size (as standard ellipse area [SEAc]) and assessing the relative placement of common sponge species in bivariate (δ13C and δ15N) plots. Sponges for this study were collected from the relatively isolated reefs within the Miskito Cays of Honduras. These reefs support diverse communities of HMA and LMA species that together span a gradient of photosymbiont abundance, as revealed by chlorophyll a analysis. HMA sponges occupied unique niche space compared to LMA species, but the placement of some HMA sponges was driven by photosymbiont abundance. In addition, photosymbiont abundance explained a significant portion of the variation in isotope values, suggesting that access to autotrophic metabolism provided by photosymbionts is an important predictor in the location of species within isotopic space. Host identity accounted for over 70% of the variation in isotope values within the Miskito Cays and there was substantial variation in the placement of individual species within isotopic niche space, suggesting that holobiont metabolic diversity may allow taxonomically diverse sponge species to utilize unique sources of nutrients within a reef system. This study provides initial evidence that microbial symbionts allow sponges to expand into novel physiochemical niche space. This expansion may reduce competitive interactions within coral reefs and promote diversification of these communities.

Highlights

By expanding the metabolic repertoires of foundational species, symbiotic interactions represent important processes underlying some of the most biodiverse ecosystemsHow to cite this article Freeman et al (2014), Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras
This study supports the contention that biogeochemical cycling of C and N is highly variable across sponge species and provides initial evidence that this variation is driven more by host species identity than by overall symbiont abundance. These reefs within the Miskito Cays of Honduras support diverse sponge communities that are taxonomically similar to those of other Caribbean reefs (Dıaz, 2005; Erwin & Thacker, 2007; Chollett, Stoyle & Box, 2014) and include species hosting both abundant and sparse microbial taxa (HMA and LMA, respectively; Thacker & Freeman, 2012). Species from this region spanned a striking gradient of photosymbiont abundance (Erwin & Thacker, 2007) with some, but not all HMA sponges support abundant photosymbiont communities
Symbionts within HMA species appear to increase holobiont metabolic diversity, leading to broader niche area (SEAc) than that observed in LMA species (Boucher, James & Keeler, 1982; Vrijenhoek, 2010)

Summary

Introduction

By expanding the metabolic repertoires of foundational species, symbiotic interactions represent important processes underlying some of the most biodiverse ecosystemsHow to cite this article Freeman et al (2014), Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. While some sponge hosts support abundant and diverse symbiont communities (termed High Microbial Abundance [HMA]), other sympatric sponge species only host sparse symbiont communities (termed Low Microbial Abundance [LMA]) (Webster et al, 2010; Schmitt et al, 2012; Thacker & Freeman, 2012; Gloeckner et al, 2014). Many of these HMA species are able to assimilate both inorganic and organic sources of C and N, whereas LMA sponges may be restricted to feeding heterotrophically on specific portions of the particulate organic matter (POM) pool in the water column (Thurber, 2007; Taylor et al, 2007; Maldonado, Ribes & van Duyl, 2012; Thacker & Freeman, 2012). With increasing evidence supporting the assimilation of dissolved organic matter (DOM) (Maldonado, Ribes & van Duyl, 2012; de Goeij et al, 2013), it is apparent that there is substantial metabolic diversity across sympatric sponge species

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