Journal of Experimental Marine Biology and Ecology
The nature and taxonomic composition of coral symbiomes as drivers of performance limits in scleractinian corals
Highlights
► We describe corals as symbiomes, multispecies super-organisms. ► Symbiomes encompass all enduring associations bounded by the coral colony. ► Symbiome complexity and function reflect habitat diversity. ► Interaction states in symbiomes are dynamic over space, time and environment. ► Symbiome complexity links to environmental sensitivity.
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.
Section snippets
Defining the functional unit in corals
The universal importance of symbiotic associations to organism (and ecosystem) function is broadly recognized (McFall-Ngai, 2008). Defining what comprises a biological individual and what contributes to its functional limits is complicated in any system, but is particularly challenging in corals because they are architecturally complex and morphologically variable, and the peripheral limits of the colony encompass a variety of compartments with very different environmental characteristics (e.g.
Architectural complexity and capacity of corals to provision habitat
The architectural complexity (micro and macro) of coral colonies creates a diversity of potentially unique habitats, a feature that will directly influence the capacity of a colony to interact with or host other species. The idea that corals represent symbiomes, or individuals whose functional attributes reflect the collective performance limits set by the multispecies assemblage they host, is provocative when one considers the implications of the level of architectural variability among and
Functional attributes associated with multispecies assemblages in corals
Research of the past decade has provided tantalizing evidence for the coral symbiome, or multispecies phenotype, to fulfill functional niches. Symbionts often provide their hosts with functional capacity that the host does not innately possess, and this extension of biological range has the potential to influence the overall success, fitness and competitive advantage of the symbiotic unit. In corals, these functional benefits include the provisioning and cycling of nutrients, defense, and
Summary
Much of the effort over the last 20 years has focused on describing patterns of diversity in a few members of the symbiotic assemblages hosted by corals across a variety of spatial scales. This work is heavily weighted to the endo- and exo-symbiotic microbial diversity in corals, with an emphasis on endosymbiotic dinoflagellates, the characterization of virus-like particles and viral sequences (Davy and Patten, 2007, Patten et al., 2008, Seymour et al., 2005), and the identification of potential
Acknowledgments
This discussion evolved while Ruth Gates was Center Fellow at the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (Grant #EF-0553768), the University of California, Santa Barbara, and the State of California, and Tracy Ainsworth was supported by Australian Research Council (DP0877226). The data sources that originally stimulated this discussion were supported by funds provided by the NSF (OCE-0752604 to RDG and NSF 04–17412 in support of the Moorea Coral Reef Long
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