Heat stress differentially impacts key calcification mechanisms in reef-building corals

Coral Reefs - Coral reefs are increasingly threatened by climate change, mass bleaching events and ocean acidification (OA). Coral calcification, a process that is critical to build and maintain...     

Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites

Background  

Corals are notoriously difficult to identify at the species-level due to few diagnostic characters and variable skeletal morphology. This 'coral species problem' is an impediment to understanding the evolution and biodiversity of this important and threatened group of organisms. We examined the evolution of the nuclear ribosomal internal transcribed spacer (ITS) and mitochondrial markers (COI, putative control region) in Porites, one of the most taxonomically challenging and ecologically important genera of reef-building corals.     

Conservation genetics and the resilience of reef-building corals

Coral reefs have suffered long-term decline due to a range of anthropogenic disturbances and are now also under threat from climate change. For appropriate management of these vulnerable and valuable ecosystems it is important to understand the factors and processes that determine their resilience and that of the organisms inhabiting them, as well as those that have led to existing patterns of coral reef biodiversity. The scleractinian (stony) corals deposit the structural framework that supports and promotes the maintenance of biological diversity and complexity of coral reefs, and as such, are major components of these ecosystems. The success of reef-building corals is related to their obligate symbiotic association with dinoflagellates of the genus Symbiodinium. These one-celled algal symbionts (zooxanthellae) live in the endodermal tissues of their coral host, provide most of the host's energy budget and promote rapid calcification. Furthermore, zooxanthellae are the main primary producers on coral reefs due to the oligotrophic nature of the surrounding waters. In this review paper, we summarize and critically evaluate studies that have employed genetics and/or molecular biology in examining questions relating to the evolution and ecology of reef-building corals and their algal endosymbionts, and that bear relevance to coral reef conservation. We discuss how these studies can focus future efforts, and examine how these approaches enhance our understanding of the resilience of reef-building corals.     

Sensitivity of calcification to thermal stress varies among genera of massive reef-building corals

Reductions in calcification in reef-building corals occur when thermal conditions are suboptimal, but it is unclear how they vary between genera in response to the same thermal stress event. Using densitometry techniques, we investigate reductions in the calcification rate of massive Porites spp. from the Great Barrier Reef (GBR), and P. astreoides, Montastraea faveolata, and M. franksi from the Mesoamerican Barrier Reef (MBR), and correlate them to thermal stress associated with ocean warming. Results show that Porites spp. are more sensitive to increasing temperature than Montastraea, with calcification rates decreasing by 0.40 g cm(-2) year(-1) in Porites spp. and 0.12 g cm(-2) year(-1) in Montastraea spp. for each 1°C increase. Under similar warming trends, the predicted calcification rates at 2100 are close to zero in Porites spp. and reduced by 40% in Montastraea spp. However, these predictions do not account for ocean acidification. Although yearly mean aragonite saturation (Ω(ar)) at MBR sites has recently decreased, only P. astreoides at Chinchorro showed a reduction in calcification. In corals at the other sites calcification did not change, indicating there was no widespread effect of Ω(ar) changes on coral calcification rate in the MBR. Even in the absence of ocean acidification, differential reductions in calcification between Porites spp. and Montastraea spp. associated with warming might be expected to have significant ecological repercussions. For instance, Porites spp. invest increased calcification in extension, and under warming scenarios it may reduce their ability to compete for space. As a consequence, shifts in taxonomic composition would be expected in Indo-Pacific reefs with uncertain repercussions for biodiversity. By contrast, Montastraea spp. use their increased calcification resources to construct denser skeletons. Reductions in calcification would therefore make them more susceptible to both physical and biological breakdown, seriously affecting ecosystem function in Atlantic reefs.     

Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals

In a coral-algae symbiotic system, heat-dependent photoinhibition of photosystem II (PSII) leads to coral bleaching. When the reef-building coral Acropora digitifera was exposed to light, a moderate increase of temperature induced coral bleaching through photobleaching of algal pigments, but not through expulsion of symbiotic algae. Monitoring of PSII photoinhibition revealed that heat-dependent photoinhibition was ascribed to inhibition of the repair of photodamaged PSII, and heat susceptibility of the repair machinery varied among coral species. We conclude that the efficiency of the photosynthesis repair machinery determines the bleaching susceptibility of coral species under elevated seawater temperatures.     

The presence of multiple phenoloxidases in Caribbean reef-building corals

The melanin-synthesis pathways, phenoloxidase (PO) and laccases, are staple components of invertebrate immunity and have been shown to be vital in disease resistance. The importance of this pathway in immunity is a consequence of the release of oxygen radicals with cytotoxic effects and the production of insoluble melanin, which aids in the encapsulation of pathogens and parasites. Recently, melanization has been demonstrated as a critical immune response in several coral systems, although the biochemical components have not been thoroughly investigated. Coral diseases are posing a serious threat to coral reef survival, necessitating a full understanding of resistance mechanisms. In this study, we take a comparative approach to probe potential pathway components of melanin-synthesis in seven species from four different families of healthy Caribbean reef-building corals. Using different quinone substrates, we tested for the activity of the POs catecholase and cresolase, as well as laccase activity in each coral species. Since many invertebrate POs demonstrate some dependence on cations such as copper, calcium and magnesium, we treated the coral extracts with the chelators EDTA and EGTA to test the reliance of coral catecholase on these cations. The activity of the antioxidants peroxidase, superoxide dismutase and catalase was also tested in each coral and correlated to PO activity. All corals had demonstrable catecholase, cresolase and laccase activities, but only catecholase and cresolase activities varied significantly among species. Catecholase activity in each coral species was reduced by treatment with EDTA and EGTA, although some coral species were less affected than the others. Overall, these data show remarkable heterogeneity among the seven coral species of boulder-like reef building Caribbean coral. These differences may originate from the level of investment of each coral species into immunity and may explain disease ecology on the reef.     

Transmission of growth anomalies between Indo-Pacific Porites corals

In this study we provide experimental evidence of transmission of growth anomalies (GAs) between corals. Twenty-four aquaria (16 experimental, 8 containing only apparently healthy corals) were set-up on Negros Island, Philippines, to test for direct-contact and waterborne transmission of GAs. Within seven weeks, two of 16 apparently healthy colonies placed in direct contact with colonies having GAs developed multiple GA lesions whose size and number increased over time. One of 16 apparently healthy colonies in experimental aquaria not touching any diseased colony also developed a GA, exhibiting a single lesion that did not increase in size. Apparently healthy colonies (n=24) in aquaria without a diseased colony remained unchanged.     

Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata

There is an ongoing debate on the scale of pelagic larval dispersal in promoting connectivity among populations of shallow, benthic marine organisms. The linearly arranged Hawaiian Islands are uniquely suited to study scales of population connectivity and have been used extensively as a natural laboratory in terrestrial systems. Here, we focus on Hawaiian populations of the lobe coral Porites lobata, an ecosystem engineer of shallow reefs throughout the Pacific. Patterns of recent gene flow and population structure in P. lobata samples (n = 318) from two regions, the Hawaiian Islands (n = 10 sites) and from their nearest neighbour Johnston Atoll, were analysed with nine microsatellite loci. Despite its massive growth form, ～ 6% of the samples from both regions were the product of asexual reproduction via fragmentation. Cluster analysis and measures of genetic differentiation indicated that P. lobata from the Hawaiian Islands are strongly isolated from those on Johnston Atoll (F(ST) = 0.311; P < 0.001), with the descendants of recent migrants (n = 6) being clearly identifiable. Within the Hawaiian Islands, P. lobata conforms to a pattern of isolation by distance. Here, over 37% (P = 0.001) of the variation in genetic distance was explained by geographical distance. This pattern indicates that while the majority of ongoing gene flow in Hawaiian P. lobata occurs among geographically proximate reefs, inter-island distances are insufficient to generate strong population structure across the archipelago.     

Widespread association of a Rickettsiales-like bacterium with reef-building corals

White band disease type I (WBD I) has been a major cause of the dramatic decline of Acroporid coral populations throughout the Caribbean during the last two decades, yet the aetiological agent of this disease is unknown. In this study, the bacterial communities associated with both healthy and diseased Acropora species were compared by 16S rDNA analyses. The bacterial communities of both healthy and diseased Acropora spp. were dominated by a single ribotype with 90% identity to a bacterium in the order Rickettsiales. Screening by nested PCR specific to the coral-associated Rickettsiales 1 (CAR1) bacterium showed that this microbe was widespread in both healthy and diseased A. cervicornis and A. palmata corals from 'healthy' (i.e. low WBD I incidence) and 'stressed' reefs (i.e. high WBD I incidence). These results indicate that there were no dramatic changes in the composition of the microbial community associated with WBD I. CAR1 was also associated with non-Acroporid corals of the Caribbean, as well as with two Acroporid corals native to the Pacific. CAR1 was not present in the water column. This bacterium was also absent from preserved Caribbean Acroporid samples collected between 1937 and 1980 before the outbreak of WBD I. These results suggest CAR1 is a relatively new bacterial associate of Acroporids and that a non-bacterial pathogen might be the cause of WBD I.     

Skeletal records of community-level bleaching in Porites corals from Palau

Tropical Pacific sea surface temperature is projected to rise an additional 2–3 °C by the end of this century, driving an increase in the frequency and intensity of coral bleaching. With significant global coral reef cover already lost due to bleaching-induced mortality, efforts are underway to identify thermally tolerant coral communities that might survive projected warming. Massive, long-lived corals accrete skeletal bands of anomalously high density in response to episodes of thermal stress. These “stress bands” are potentially valuable proxies for thermal tolerance, but to date their application to questions of community bleaching history has been limited. Ecological surveys recorded bleaching of coral communities across the Palau archipelago during the 1998 and 2010 warm events. Between 2011 and 2015, we extracted skeletal cores from living Porites colonies at 10 sites spanning barrier reef and lagoon environments and quantified the proportion of stress bands present in each population during bleaching years. Across Palau, the prevalence of stress bands tracked the severity of thermal stress, with more stress bands occurring in 1998 (degree heating weeks = 13.57 °C-week) than during the less severe 2010 event (degree heating weeks = 4.86 °C-week). Stress band prevalence also varied by reef type, as more corals on the exposed barrier reef formed stress bands than did corals from sheltered lagoon environments. Comparison of Porites stress band prevalence with bleaching survey data revealed a strong correlation between percent community bleaching and the proportion of colonies with stress bands in each year. Conversely, annual calcification rates did not decline consistently during bleaching years nor did annually resolved calcification histories always track interannual variability in temperature. Our data suggest that stress bands in massive corals contain valuable information about spatial and temporal trends in coral reef bleaching and can aid in conservation efforts to identify temperature-tolerant coral reef communities.

     

Growth characteristics of the reef-building coral Porites astreoides under different environmental conditions in the Western Atlantic

Skeletal extension (3.67 ± 0.65 mm year⁻¹), density (1.49 ± 0.16 g cm⁻³), and calcification rate (0.55 ± 0.12 g cm⁻² year⁻¹) were determined using annual growth bands of Porites astreoides skeletons collected in three different reef systems in the Western Atlantic. The corals showed a low-density annual growth band at their apex, and seasonal timing of low and high-density band formation in P. astreoides appears to be similar at the three study sites in the Western Atlantic. The range of values presented here, for the three growth variables, spans the known range of skeletal-growth variability in P. astreoides for the Western Atlantic. The relationships between the growth parameters were similar to those previously described by other authors for massive Porites species from the Indo-Pacific, suggesting that P. astreoides has the same growth strategy, primarily investing calcification resources in extension rate. It is noteworthy that the P. astreoides population growing off the northwest coast of Cuba had similar growth characteristics as populations from the Caribbean region which were different from populations in the Gulf of Mexico, which seem to be isolated and adapted for growth at higher average sea-surface temperatures.     

Abundant betaines in reef-building corals and ecological indicators of a photoprotective role

Betaines are well known as compatible solutes that exert protein- and membrane-stabilizing effects, including protective effects on photosynthesis in plants and free-living algae stressed by high irradiance or unusual temperatures. Betaines, however, have received minimal attention in reef-building corals. One goal of this research was to identify and quantify the betaines of reef-building corals with chemically definitive methods. Metabolite profiling was conducted on 10 species (6 genera) of Curaçao corals by liquid chromatography/time-of-flight mass spectrometry calibrated using six stable-isotope-labeled internal standards. Glycine betaine (GlyB), proline betaine (ProB), alanine betaine (AlaB), β-alanine betaine, hydroxyproline betaine (HProB), taurine betaine (TauB), trigonelline (Trig) and the chemically related sulfonium compound dimethylsulfoniopropionate were found in all species. Relative levels of betaines varied across species, with GlyB and ProB being most prominent. Betaines were collectively abundant; estimated total concentrations were 12 to 204 (mean = 75) mmol per liter of tissue. A second goal was to examine ecological patterns in betaine concentrations in field populations of Curaçao corals. Betaine concentrations exhibited intraspecific patterns that matched a priori predictions for molecules that defend photosynthesis against negative effects of high irradiance. In Madracis mirabilis—which occupies unshaded locations—GlyB, ProB, AlaB, HProB, and Trig were 37–94% more abundant in colonies at 5 m depth (high irradiance) than 20 m. In M. pharensis—which occupies exposed and shaded locations—GlyB, ProB, and AlaB were 30–44% more abundant in unshaded than shaded colonies at one depth. M. senaria exhibited 45–93% increases in concentrations of betaines—GlyB, AlaB, HProB, TauB, and Trig—between early and late in the day, although M. mirabilis and pharensis did not. The results indicate that multiple betaines occur commonly in reef-building coral species, and betaine concentrations are modulated in response to growth light conditions in ways consistent with betaines acting as agents of photoprotection of coral photosynthesis.     

Contrasting Lesion Dynamics of White Syndrome among the scleractinian corals Porites spp

White syndrome (WS) is currently the most prevalent disease of scleractinian corals in the Indo-Pacific region, with an ability to exist in both epizootic and enzootic states. Here, we present results of an examination of WS lesion dynamics and show that potentially associated traits of host morphology (i.e., branching vs. massive), lesion size, and tissue deposition rate influence disease severity and recovery. Lesion healing rate was positively correlated with initial lesion size in both morphologies, but the rate at which lesions healed differed between morphologies. New lesions in branching Porites cylindrica appeared less frequently, were smaller and healed more quickly, but were more abundant than in closely-related massive Porites sp(p). The positive association between lesion size and healing rate was partly explained by geometry; branching limited lesion maximum size, and larger lesion margins contained more polyps producing new tissue, resulting in faster healing. However, massive colonies deposited tissue more slowly than branching colonies, resulting in slower recovery and more persistent lesions. Corallite size and density did not differ between species and did not, therefore, influence healing rate. We demonstrated multiple modes of pathogen transmission, which may be influenced by the greater potential for pathogen entrainment in branching vs. massive morphologies. We suggest that attributes such as colony morphology and species-specific growth rates require consideration as we expand our understanding of disease dynamics in colonial organisms such as coral.     

Short term viability of soft tissue detached from the skeleton of reef-building corals

We have induced soft tissue detachment from the skeleton of two colonial hard corals of the Pocilloporid family, both in vivo and in vitro. A parallel was made between polyp “bail-out”, i.e. field and laboratory-observed detachment of tissue fragments alone from the skeleton, and the dissociation method used for initiation of coral primary cell cultures. The in vitro approach provided insights into the active cellular re-arrangement mechanisms underlying coral tissue detachment. Functional polyps were not regenerated. Viability of tissue isolates detached from coral skeleton was probed for their use as a model for short-term biological assays. Cell viability dropped from 70% to 30% within the first week maintenance in vitro. Short-term isolate cultures limited to 3 days are a compromise allowing attachment of coral cells, yet preserving viability at about 70% of the total coral cell population.     

Sexual systems in scleractinian corals: an unusual pattern in the reef-building species Diploastrea heliopora

The sexual system in corals refers to the spatial and temporal pattern of sexual function within an individual coral polyp, colony or population. Although information on sexual systems now exists for over 400 scleractinian species, data are still lacking for some important reef-building taxa. The vast majority of scleractinians are either simultaneous hermaphrodites or gonochoric with other sexual systems rarely occurring. Diploastrea heliopora is one of the most ubiquitous and easily recognised reef-building species in the Indo-West Pacific; however, surprisingly little is known about its reproductive biology. The aim of the present study was to examine the reproductive biology of D. heliopora colonies on chronically impacted, equatorial reefs south of Singapore. Here we show that in Singapore, D. heliopora is a broadcast spawner with predominantly gonochoric polyps. Colonies, however, contained male, female and a low proportion of cosexual polyps during the 14-month sampling period. The most plausible explanation for this is that polyps switch sexes with oogenic and spermatogenic cycles occasionally overlapping. This leads to colony level alternation of sex function within and between breeding seasons. While this sexual system is atypical for scleractinians, it supports molecular evidence that D. heliopora is phylogenetically distinct from species formerly in the family Faviidae.     

Species richness and community structure of reef-building corals on the nearshore Great Barrier Reef

Species richness, cover and community structure of reef-building corals were assessed at 599 sites on 135 reefs along the Great Barrier Reef (GBR) between 1994 and 2001, with focus on the nearshore area. Communities were described hierarchically, with smaller regional communities forming part of higher level communities at increasing spatial scales. Site richness increased from the coast to the mid-continental shelf, declining on the outer shelf. Richness also increased with depth to 5 m, stabilizing thereafter. An anomaly was present in a 400 km section adjacent to the northern, ‘wet tropics’ coast, where site richness was 67 and 41% lower than the adjacent far northern and central GBR, respectively; this was probably due to the disturbance regime, with an apparent anthropogenic component. Site richness also declined in the Southern GBR, probably due to naturally marginal conditions. All indicator species had highest values in five small Far Northern and Central GBR communities. In the eight depauperate communities no indicator species had high values, indicating that these communities represent degraded, yet potentially transitional forms of the more diverse communities of the Far Northern and Central GBR. The study shows that on the GBR, disturbance results in the local removal of corals rather than a shift to suites of other coral species.     

Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types

The photobiology of two reef corals and the distribution of associated symbiont types were investigated over a depth gradient of 0-60 m at Scott Reef, Western Australia. Pachyseris speciosa hosted mainly the same Symbiodinium C type similar to C3 irrespective of sampling depth. By contrast, Seriatopora hystrix hosted predominantly Symbiodinium type D1a or D1a-like at shallow depths while those in deeper water were dominated by a Symbiodinium C type closely related to C1. The photosynthesis/respiration (P/R) ratio increased consistently with depth at the two sampling times (November 2008 and April 2009) for P. speciosa and in November 2008 only for S. hystrix, suggesting a reduction in metabolic energy expended for every unit of energy obtained from photosynthesis. However, in April 2009, shallow colonies of S. hystrix exhibited decreased P/R ratios down to depths of approximately 23 m, below which the ratio increased towards the maximum depth sampled. This pattern was mirrored by changes in tissue biomass determined as total protein content. The depth of change in the direction of the P/R ratio correlated with a shift from Symbiodinium D to C-dominated colonies. We conclude that while photobiological flexibility is vital for persistence in contrasting light regimes, a shift in Symbiodinium type may also confer a functional advantage albeit at a metabolic cost with increased depth.     

Quantification of virus-like particles suggests viral infection in corals affected by Porites tissue loss

Porites tissue loss is a common disease of Porites compressa on Hawaiian reefs. Despite its prevalence, to date, the aetiological agent of the disease has not been found. The apparent lack of a microbial causative agent in the similar disease Porites bleaching with tissue loss, as well as increasing evidence of viral infections in scleractinian corals and Symbiodinium, led us to hypothesise that a virus may be responsible. Electron microscopy revealed the presence of numerous and varied virus-like particles (VLPs) in healthy and diseased P. compressa colonies. While overall virus numbers were similar in all samples, the abundance of a group of icosahedral VLPs differed significantly between healthy and diseased colonies. While not conclusive, these results suggest that viruses may play a role in this disease, and provide a basis for further studies.     

Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals

Background

Coral reefs worldwide are in decline. Much of the mortality can be attributed to coral bleaching (loss of the coral''s intracellular photosynthetic algal symbiont) associated with global warming. How corals will respond to increasing oceanic temperatures has been an area of extensive study and debate. Recovery after a bleaching event is dependent on regaining symbionts, but the source of repopulating symbionts is poorly understood. Possibilities include recovery from the proliferation of endogenous symbionts or recovery by uptake of exogenous stress-tolerant symbionts.

Methodology/Principal Findings

To test one of these possibilities, the ability of corals to acquire exogenous symbionts, bleached colonies of Porites divaricata were exposed to symbiont types not normally found within this coral and symbiont acquisition was monitored. After three weeks exposure to exogenous symbionts, these novel symbionts were detected in some of the recovering corals, providing the first experimental evidence that scleractinian corals are capable of temporarily acquiring symbionts from the water column after bleaching. However, the acquisition was transient, indicating that the new symbioses were unstable. Only those symbiont types present before bleaching were stable upon recovery, demonstrating that recovery was from the resident in situ symbiont populations.

Conclusions/Significance

These findings suggest that some corals do not have the ability to adjust to climate warming by acquiring and maintaining exogenous, more stress-tolerant symbionts. This has serious ramifications for the success of coral reefs and surrounding ecosystems and suggests that unless actions are taken to reverse it, climate change will lead to decreases in biodiversity and a loss of coral reefs.