More than local adaptation: high diversity of response to seawater acidification in seven coral species from the same assemblage in French Polynesia

Responses of corals to seawater acidification have been extensively studied. Sensitivity varies widely between species, highlighting the need to avoid extrapolation from one to another to get an accurate understanding of coral community responses. We tested the responses of seven coral species (Acropora cytherea, Acropora hyacinthus, Acropora pulchra, Leptastrea pruinosa, Montipora grisea, Pavona cactus, Pocillopora verrucosa) from the Mo'orea lagoon to a 48-day exposure to three pH scenarios (pH 7.95, 7.7 and 7.3). Tissue necrosis, mortality, growth rates, photophysiological performances and colour index were recorded. Few significant differences were noted between pH 7.95 and 7.7, but species-specific responses were observed at pH 7.3. While our data do not allow identification of the mechanisms behind this diversity in response between species inhabiting the same environment, it can exclude several hypotheses such as local adaptation, skeletal type, corallum morphology or calcification rate as sole factors determining coral sensitivity to pH.

Improper Diving Behavior Affects Physiological Responses of Acropora hyacinthus and Porites cylindrica

Human activities beyond ecosystem capacity have resulted in serious effects on corals worldwide. Nowadays, many studies have focused on the influence of diving activities on coral communities, while the knowledge of physiological changes under corresponding environmental stresses remains largely undetermined. In the study, we aimed to investigate the physiological effects of touching, ammonia nitrogen enrichment (5 μmol⋅L–1), and sediment cover (particle size of less than 0.3 mm), which simulated improper self-contained underwater breathing apparatus (SCUBA) diving behaviors, on Acropora hyacinthus and Porites cylindrica in Wuzhizhou Island, the South China Sea. For A. hyacinthus, continuous touching caused the tentacles to shrink and secrete mucus, which consumed energy and dissolved oxygen. The skeletal growth rate was decreased by 72% compared with the control group. There was a rapid decline of Fv/Fm and alpha under the dual impacts of high ammonia nitrogen and touching, while the Chl a concentration and tissue biomass were decreased by 36 and 28% compared with touching alone, respectively. High ammonia nitrogen and touching increased the concentrations of lipid and protein. Nevertheless, zooxanthellae density was increased by 23% to relieve the effects of a lower concentration of Chl a in a high nutrient environment. Constant touching and sediment cover in diving areas with elevated ammonia content affected the photosynthesis and respiration of corals, and a significant decrease was observed for lipid, zooxanthellae density, and Chl a concentration. Coral bleaching occurred on day 7. For P. cylindrica, the decreasing magnitude of Fv/Fm and alpha under different stresses in the subsequent phase was less compared with A. hyacinthus. The contents of carbohydrate and protein under continuous touching were decreased by 7 and 15% compared with the control group, respectively, causing negative growth. Under the dual influences of high ammonia nitrogen and continuous touching, all energy reserves were significantly lower. Repeated touching and sediment cover in diving areas containing high ammonia content increased the concentrations of lipid and protein compared with the touching and high nutrient treatment group likely because that Porites associated with C15 zooxanthella increased heterotrophic feeding to compensate for restricted symbiodiniaceae photosynthesis. Additionally, P. cylindrica produced mucus to aid the removal of sediment, so that corals didn’t obviously bleach during the experiment. Collectively, P. cylindrica was more resistant to diving activities than A. hyacinthus which only relies on photoautotrophy. To ensure the sustainable development of coral reef dive tourism, it is necessary to strengthen the supervision of diving behaviors, rotate the diving areas, and conduct regular assessments on the coral status.

Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral Acropora hyacinthus in Palau

Climate change is dramatically changing ecosystem composition and productivity, leading scientists to consider the best approaches to map natural resistance and foster ecosystem resilience in the face of these changes. Here we present results from a large-scale experimental assessment of coral bleaching resistance, a critical trait for coral population persistence as oceans warm, in 221 colonies of the coral Acropora hyacinthus across 37 reefs in Palau. We find that bleaching resistant individuals inhabit most reefs but are found more often in warmer microhabitats. Our survey also found wide variation in symbiont concentration among colonies, and that colonies with lower symbiont load tended to be more bleaching resistant. By contrast, our data show that low symbiont load comes at the cost of lower growth rate, a tradeoff that may operate widely among corals across environments. Corals with high bleaching resistance have been suggested as a source for habitat restoration or selective breeding in order to increase coral reef resilience to climate change. Our maps show where these resilience corals can be found, but the existence of tradeoffs with heat resistance may suggest caution in unilateral use of this one trait in restoration.

Demographic Inferences and Loci Under Selection in a Recently Expanded Coral Population

Coral poleward range expansions in response to warming oceans have been historically observed, however contemporary expansion rates of some coral species have become more rapid as global temperatures rise at unprecedented rates. Range expansion can lead to reduced genetic diversity and surfing of deleterious mutations in expanding populations, potentially limiting the ability for adaption and persistence in novel environments. Successful expansions that overcome these founder effects and colonize new habitat have been attributed to multiple introductions from different sources, hybridization with native populations, or rapid adaptive evolution. Here, we investigate population genomic patterns of the reef-building coral Acropora hyacinthus along a latitudinal cline that includes a well-established range expansion front in Japan using 2b-RAD sequencing. A total of 184 coral samples were collected across seven sites spanning from ~24N to near its northern range front at ~33N. We uncover the presence of three cryptic lineages of A. hyacinthus, which occupy discrete areas within this region. Only one lineage is present at the expansion front and we find evidence of its historical occupation of marginal habitats. Within this lineage we also find evidence of bottleneck pressures associated with expansion events including higher clonality, increased linkage disequilibrium, and lower genetic diversity in range edge populations compared to core populations. Asymmetric migration between populations was also detected with lower migration from edge sites. Lastly, we describe genomic signatures of local adaptation potentially attributed to lower winter temperatures experienced at the more recently expanded northern populations. Together these data illuminate the genomic consequences of range expansion in a coral and highlight how adaptation to colder temperatures along the expansion front may facilitate further range expansion in this coral lineage.

Species-Specific Variations in the Metabolomic Profiles of Acropora hyacinthus and Acropora millepora Mask Acute Temperature Stress Effects in Adult Coral Colonies

Coral reefs are suffering unprecedented declines in health state on a global scale. Some have suggested that human assisted evolution or assisted gene flow may now be necessary to effectively restore reefs and pre-condition them for future climate change. An understanding of the key metabolic processes in corals, including under stressed conditions, would greatly facilitate the effective application of such interventions. To date, however, there has been little research on corals at this level, particularly regarding studies of the metabolome of Scleractinian corals. Here, the metabolomic profiles [measured using 1H nuclear magnetic resonance spectroscopy (1H NMR) and ultra-high-performance liquid chromatography-mass spectrometry (LC-MS)] of two dominant reef building corals, Acropora hyacinthus and A. millepora, from two distinct geographical locations (Australia and Singapore) were characterized. We assessed how an acute temperature stress (an increase of 3.25°C ± 0.28 from ambient control levels over 8 days), shifted the corals’ baseline metabolomic profiles. Regardless of the profiling method utilized, metabolomic signatures of coral colonies were significantly distinct between coral species, a result supporting previous work. However, this strong species-specific metabolomic signature appeared to mask any changes resulting from the acute heat stress. On closer examination, we were able to discriminate between control and temperature stressed groups using a partial least squares discriminant analysis classification model (PLSDA). However, in all cases “late” components needed to be selected (i.e., 7 and 8 instead of 1 and 2), suggesting any treatment effect was small, relative to other sources of variation. This highlights the importance of pre-characterizing the coral colony metabolomes, and of factoring that knowledge into any experimental design that seeks to understand the apparently subtle metabolic effects of acute heat stress on adult corals. Further research is therefore needed to decouple these apparent individual and species-level metabolomic responses to climate change in corals.

Codominance of two symbiont genera within the same coral host is associated with elevated symbiont productivity and lower host susceptibility to thermal stress

As sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this has on the host. We used previously published data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportions of symbiont genera within the host. We find that both Cladocopium and Durusdinium change their expression most when their proportions are nearly equal (the state that we call “codominance”): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two ways. One explanation is that increased competition between symbionts heightens their productivity, which benefits the host, making it more resilient to stress. Alternatively, the symbionts’ elevated productivity might be the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbionts’ competition and allowing for codominance. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities. Irrespective of the causation, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

Codominance of two symbiont genera within the same coral host is associated with elevated symbiont productivity and lower host susceptibility to thermal stress

In recent years, as sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how the symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this interaction has on the host. We used previously published transcriptomic data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportion of the two symbiont genera within the same host. We find that both Cladocopium and Durusdinium change their expression the most when their proportions within the host are nearly equal (the state that we call “codominance”): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two alternative ways. One explanation is that increased competition between codominant symbionts switches them to the higher productivity mode, which benefits the host, making it more resilient to stress. Alternatively, the symbionts’ elevated productivity might be not the cause but the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbioints’ competition and thus promoting their growth, which allows for codominance to happen where one genus would otherwise outcompete another. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities, assessed as relative proportions of symbiont reads in the data. Irrespective of the causation direction, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

Coral growth, survivorship and return-on-effort within nurseries at high-value sites on the Great Barrier Reef

Coral reefs are deteriorating worldwide prompting reef managers and stakeholders to increasingly explore new management tools. Following back-to-back bleaching in 2016/2017, multi-taxa coral nurseries were established in 2018 for the first time on the Great Barrier Reef (GBR) to aid reef maintenance and restoration at a “high-value” location–Opal Reef–frequented by the tourism industry. Various coral species (n = 11) were propagated within shallow water (ca. 4-7m) platforms installed across two sites characterised by differing environmental exposure–one adjacent to a deep-water channel (Blue Lagoon) and one that was relatively sheltered (RayBan). Growth rates of coral fragments placed onto nurseries were highly variable across taxa but generally higher at Blue Lagoon (2.1–10.8 cm2 month-1 over 12 months) compared to RayBan (0.6–6.6 cm2 month-1 over 9 months). Growth at Blue Lagoon was largely independent of season, except for Acropora tenuis and Acropora hyacinthus, where growth rates were 15–20% higher for December 2018-July 2019 (“warm season”) compared to August-December 2018 (“cool season”). Survivorship across all 2,536 nursery fragments was ca. 80–100%, with some species exhibiting higher survivorship at Blue Lagoon (Acropora loripes, Porites cylindrica) and others at RayBan (A. hyacinthus, Montipora hispida). Parallel measurements of growth and survivorship were used to determine relative return-on-effort (RRE) scores as an integrated metric of “success” accounting for life history trade-offs, complementing the mutually exclusive assessment of growth or survivorship. RRE scores within sites (across species) were largely driven by growth, whereas RRE scores between sites were largely driven by survivorship. The initial nursery phase of coral propagation therefore appears useful to supplement coral material naturally available for stewardship of frequently visited Great Barrier Reef tourism (high-value) sites, but further assessment is needed to evaluate how well the growth rates and survival for nursery grown corals translate once material is outplanted.

Energy depletion and opportunistic microbial colonisation in white syndrome lesions from corals across the Indo-Pacific

Corals are dependent upon lipids as energy reserves to mount a metabolic response to biotic and abiotic challenges. This study profiled lipids, fatty acids, and microbial communities of healthy and white syndrome (WS) diseased colonies of Acropora hyacinthus sampled from reefs in Western Australia, the Great Barrier Reef, and Palmyra Atoll. Total lipid levels varied significantly among locations, though a consistent stepwise decrease from healthy tissues from healthy colonies (HH) to healthy tissue on WS-diseased colonies (HD; i.e. preceding the lesion boundary) to diseased tissue on diseased colonies (DD; i.e. lesion front) was observed, demonstrating a reduction in energy reserves. Lipids in HH tissues were comprised of high energy lipid classes, while HD and DD tissues contained greater proportions of structural lipids. Bacterial profiling through 16S rRNA gene sequencing and histology showed no bacterial taxa linked to WS causation. However, the relative abundance of Rhodobacteraceae-affiliated sequences increased in DD tissues, suggesting opportunistic proliferation of these taxa. While the cause of WS remains inconclusive, this study demonstrates that the lipid profiles of HD tissues was more similar to DD tissues than to HH tissues, reflecting a colony-wide systemic effect and provides insight into the metabolic immune response of WS-infected Indo-Pacific corals.