Effective marine management requires comprehensive data on the status of marine biodiversity. However, efficient methods that can document biodiversity in our oceans are currently lacking. Environmental DNA (eDNA) sourced from seawater offers a new avenue for investigating the biota in marine ecosystems. Here, we investigated the potential of eDNA to inform on the breadth of biodiversity present in a tropical marine environment. Directly sequencing eDNA from seawater using a shotgun approach resulted in only 0.34% of 22.3 million reads assigning to eukaryotes, highlighting the inefficiency of this method for assessing eukaryotic diversity. In contrast, using ‘tree of life’ (ToL) metabarcoding and 20-fold fewer sequencing reads, we could detect 287 families across the major divisions of eukaryotes. Our data also show that the best performing ‘universal’ PCR assay recovered only 44% of the eukaryotes identified across all assays, highlighting the need for multiple metabarcoding assays to catalogue biodiversity. Lastly, focusing on the fish genus Lethrinus, we recovered intra- and inter-specific haplotypes from seawater samples, illustrating that eDNA can be used to explore diversity beyond taxon identifications. Given the sensitivity and low cost of eDNA metabarcoding we advocate this approach be rapidly integrated into biomonitoring programs.
Symbioses are widespread in nature and occur along a continuum from parasitism to mutualism. Coral-dinoflagellate symbioses are defined as mutualistic because both partners receive benefit from the association via the exchange of nutrients. This successful interaction underpins the growth and formation of coral reefs. The symbiotic dinoflagellate genus Symbiodinium is genetically diverse containing eight divergent lineages (clades A-H). Corals predominantly associate with clade C Symbiodinium and to a lesser extent with clades A, B, D, F, and G. Variation in the function and interactive physiology of different coral-dinoflagellate assemblages is virtually unexplored but is an important consideration when developing the contextual framework of factors that contribute to coral reef resilience. In this study, we present evidence that clade A Symbiodinium are functionally less beneficial to corals than the dominant clade C Symbiodinium and may represent parasitic rather than mutualistic symbionts. Our hypothesis is supported by (i) a significant correlation between the presence of Symbiodinium clade A and health-compromised coral; (ii) a phylogeny and genetic diversity within Symbiodinium that suggests a different evolutionary trajectory for clade A compared with the other dominant Symbiodinium lineages; and (iii) a significantly lower amount of carbon fixed and released by clade A in the presence of a coral synthetic host factor as compared with the dominant coral symbiont lineage, clade C. Collectively, these data suggest that along the symbiotic continuum the interaction between clade A Symbiodinium and corals may be closer to parasitism than mutualism.cnidaria ͉ Symbiodinium ͉ disease ͉ mutualistic ͉ parasitic
Abstract. Most studies on coral reefs have focused on shallow reef (,30 m) systems due to the technical limitations of conducting scientific diving deeper than 30 m. Compared to their shallow-water counterparts, these mesophotic coral reefs (30-150 m) are understudied, which has slowed our broader understanding of the biodiversity, ecology, and connectivity of shallow and deep coral reef communities. We know that the light environment is an important component of the productivity, physiology, and ecology of corals, and it restricts the distribution of most species of coral to depths of 60 m or less. In the Bahamas, the coral Montastraea cavernosa has a wide depth distribution, and it is one of the most numerous corals at mesophotic depths. Using a range of optical, physiological, and biochemical approaches, the relative dependence on autotrophy vs. heterotrophy was assessed for this coral from 3 to 91 m. These measurements show that the quantum yield of PSII fluorescence increases significantly with depth for M. cavernosa while gross primary productivity decreases with depth. Both morphological and physiological photoacclimatization occurs to a depth of 91 m, and stable isotope data of the host tissues, symbionts, and skeleton reveal a marked decrease in productivity and a sharp transition to heterotrophy between 45 and 61 m. Below these depths, significant changes in the genetic composition of the zooxanthellae community, including genotypes not previously observed, occur and suggest that there is strong selection for zooxanthellae that are suited for survival in the light-limited environment where mesophotic M. cavernosa are occurring.
Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.
Flexibility in biological systems is seen as an important driver of macro-ecosystem function and stability. Spatially constrained endosymbiotic settings, however, are less studied, although environmental thresholds of symbiotic corals are linked to the function of their endosymbiotic dinoflagellate communities. Symbiotic flexibility is a hypothesized mechanism that corals may exploit to adapt to climate change. This study explores the flexibility of the coral-Symbiodinium symbiosis through quantification of Symbiodinium ITS2 sequence assemblages in a range of coral species and genera. Sequence assemblages are expressed as an index of flexibility incorporating phylogenetic divergence and relative abundance of Symbiodinium sequences recovered from the host. This comparative analysis reveals profound differences in the flexibility of corals for Symbiodinium, thereby classifying corals as generalists or specifists. Generalists such as Acropora and Pocillopora exhibit high intra-and inter-species flexibility in their Symbiodinium assemblages and are some of the most environmentally sensitive corals. Conversely, specifists such as massive Porites colonies exhibit low flexibility, harbour taxonomically narrow Symbiodinium assemblages, and are environmentally resistant corals. Collectively, these findings challenge the paradigm that symbiotic flexibility enhances holobiont resilience. This underscores the need for a deeper examination of the extent and duration of the functional benefits associated with endosymbiotic diversity and flexibility under environmental stress.
Clade DSymbiodiniumare thermally tolerant coral endosymbionts that confer resistance to elevated sea surface temperature and bleaching to the host. The union between corals and clade D is thus important to management and coral conservation. Here, we review the diversity and biogeography of clade DSymbiodinium, factors linked to increasing abundances of clade D, and the benefits and drawbacks of associating with clade D for corals. We identify clade DSymbiodiniumas uncommon pandemically distributed generalists found in higher abundances on reefs exposed to challenging sea surface temperatures and local stressors or with a history of bleaching. This distribution suggests that clade DSymbiodiniumare mostly opportunistic endosymbionts, whereby they outcompete and replace optimal symbionts in health-compromised corals. We conclude by identifying research gaps that limit our understanding of the adaptive role clade DSymbiodiniumplay in corals and discuss the utility of monitoring clade DSymbiodiniumas indicators of habitat degradation in coral reef ecosystems.
Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism’s function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.
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