The nature and taxonomic composition of coral symbiomes as drivers of performance limits in scleractinian corals

Abstract

All plants and animals host complex communities of taxonomically diverse microbial assemblages (viruses, Archaea, Bacteria, micro-eukaryotes) that contribute to the functional attributes of the host organism. Scleractinian corals represent particularly provocative subjects for study in this context because they are morphologically complex and associate with a broad diversity of macro invertebrates and vertebrates as well as microorganisms. Representatives of all these taxonomic groupings have been shown to contribute to the function of corals through direct or indirect provisioning and cycling of nutrients, waste removal, defense, and stress tolerance, traits that influence the fitness and environmental thresholds of individual coral colonies. How the taxonomic composition, functional limits and interactive nature of members of these communities vary among and within host species, and scale up to influence community level processes that drive ecosystem structure and function through time and space is unknown; these communities are, however, taxonomically variable among individual corals. Here we draw on the published literature to discuss the ecological and functional significance of the broad and variable taxonomic symbioses found closely associated with corals. Using a comparative approach, we hypothesize that the intra-specific and inter-specific variations in response of corals to environmental disturbance is linked to differences in the specificity, nature and composition of these symbiotic assemblages and reflect variation in the architectural complexity (micro and macro) and capacity of corals to provision habitat. We describe individual coral colonies as symbiomes, unique micro-ecosystems bounded by the physical limits of the coral colony whose performance limits reflect the taxonomic range of the associates (micro and macro) found within the colony. We explicitly recognize the fact that corals represent complex ecological communities composed of organisms that have the potential to compete, as well as interact with one another and the host as commensals, mutualists and parasites, states that likely to be dynamic with nature, context and environment.

Introduction

Coral reefs are productive and diverse tropical marine ecosystems framed by massive three-dimensional structures created by the deposition of calcium carbonate skeletons by individual coral colonies (Goreau and Goreau, 1959). These skeletons are hugely variable in form, reflecting innate characteristics of different coral species that scale with age, and are in some cases, plastic with respect to environmental conditions (Todd, 2008). The architectural complexity created by coral communities that combine to form coral reefs, provides a plethora of habitats to support an enormous diversity of organisms from all kingdoms of life. The capacity of coral reefs to host such broad biodiversity represents a defining feature of these important coastal ecosystems (Grottoli et al., 2006, Rohwer et al., 2002, Schwarz et al., 2008, Stella et al., 2010).

Like the reef, each coral colony serves as habitat for a diverse assemblage of macro- and micro-eukaryotes, Bacteria, Archaea and viruses (Rohwer et al., 2001). This biodiversity occupies a variety of niches both within coral tissues and skeletons, closely associated with the surface of the coral and the mucus layers, and in the waters within or under the branches, lobes and plates of the coral colony (Ainsworth et al., 2010, Bourne and Munn, 2005, Lampert et al., 2006, Stella et al., 2010, Sunagawa et al., 2010). Each member of these multi-species assemblages or symbioses has the potential to interact with the coral host to a lesser or greater extent, and to contribute or detract from the overall fitness and long-term survival of the coral colony (Pratchett, 2001, Rohwer et al., 2001, Stella et al., 2010), impacts that scale up to affect reef structure and ecosystem processes (Fig. 1). We use the term symbiosis here to describe close enduring associations between individuals of different species (Bouchard, 2009) recognizing that these interactions can change in time, space and environment, to be beneficial, neutral and also negative (see Table 1 for terms and definitions). For example, functional attributes of the intimate unions between corals and unicellular dinoflagellates in the genus Symbiodinium drive high rates of productivity and calcium carbonate deposition that create the structure of the reef (Yellowlees et al., 2008). The nature and taxonomic composition of these interactions are spatially and temporally variable among and within coral species, and can be dramatically influenced by changes in the abiotic environment. Differences in the taxonomy of Symbiodinium manifest in physiological variation that influences environmental thresholds, and as such, the relative abundance of specific Symbiodinium types hosted by individual coral colonies has profound implications for the persistence of an individual coral through time, and in the face of environmental disturbance (reviewed in Stat et al., 2006).

The functional underpinnings of associations between Symbiodinium and corals are by far the most comprehensively studied to date, however, Bacteria, endolithic algae, and a diversity of invertebrates and vertebrates have also been shown to contribute to the performance of the coral by provisioning and cycling of nutrients, defending the colony and increasing thermal tolerance (e.g. Cleveland et al., 2011, Fine and Loya, 2002, Holbrook et al., 2008, Stewart et al., 2006). This suggests that the complex assemblages hosted by corals confer benefits to the coral hosts and as a collective, have the potential to contribute to the functional range, environmental thresholds and resilience of corals and reefs.

Corals exhibit high intra and inter-specific variability in response to environmental disturbance, a trait that scales up to influence reef wide ecology (Loya et al., 2001). Here we develop a discussion framed by the idea that the performance of individual corals reflects physiological limits imposed upon the colony by the combined activities of the broad taxonomic diversity of organisms found in symbiosis with each coral colony. We propose (1) that each coral can be described by the term symbiome, a polygenomic super-organism or system that encompasses all enduring associations (micro and macro) bounded by the physical limits of the colony (Sapp, 2003¹); (2) that the nature and composition of the multispecies assemblage reflect the diversity of habitats within the symbiome as well as community level process such as competition and resource limitation; (3) that the multispecies assemblages in coral symbiomes interact with each other and the host in mutualistic, commensal, and parasitic states that are potentially dynamic over space, time and environment; and, (4) that symbiomes in branching corals are more complex than in massive corals, complexity that translates into positive fitness traits (for instance growth rates) under normal conditions, but that may also contribute to the increased sensitivity to branching corals under environmental stress.