Linking photoacclimation responses and microbiome shifts between depth-segregated sibling species of reef corals

Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea, and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the Caribbean corals Orbicella annularis and O. franksi. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation, low mortality, and maintained a consistent bacterial community. In contrast, O. annularis experienced higher mortality, and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts.

Differential Response of the Microbiome of Pocillopora acuta to Reciprocal Transplantation Within Singapore

As corals continue to decline globally, particularly due to climate change, it is vital to understand the extent to which their microbiome may confer an adaptive resilience against environmental stress. Corals that survive on the urban reefs of Singapore are ideal candidates to study the association of scleractinians with their microbiome, which in turn can inform reef conservation and management. In this study, we monitored differences in the microbiome of Pocillopora acuta colonies reciprocally transplanted between two reefs, Raffles and Kusu, within the Port of Singapore, where corals face intense anthropogenic impacts. Pocillopora acuta had previously been shown to host distinct microbial communities between these two reefs. Amplicon sequencing (16S rRNA) was used to assess the coral microbiomes at 1, 2, 4, and 10 days post-transplantation. Coral microbiomes responded rapidly to transplantation, becoming similar to those of the local corals at the destination reef within one day at Raffles and within two days at Kusu. Elevated nitrate concentrations were detected at Raffles for the duration of the study, potentially influencing the microbiome’s response to transplantation. The persistence of corals within the port of Singapore highlights the ability of corals to adapt to stressful environments. Further, coral resilience appears to coincide with a dynamic microbiome which can undergo shifts in composition without succumbing to dysbiosis.

Coral bleaching response is unaltered following acclimatization to reefs with distinct environmental conditions

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change–resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine whether stress resistance is affected by transplantation beyond a coral’s native reef. Here, we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between reefs with distinct pH, salinity, dissolved oxygen, sedimentation, and flow dynamics to determine whether heat stress response is altered following coral exposure to novel physicochemical conditions in situ. Critically, transplantation had no influence on coral heat stress responses, indicating that this trait was relatively fixed. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolic rates and overall fitness were higher at the reef with higher flow, salinity, sedimentation, and diel fluctuations of pH and dissolved oxygen, and did not differ between native and cross-transplanted corals, indicating acclimatization via plasticity within just 3 mo. Conversely, cross-transplants at the second reef had higher fitness than native corals, thus increasing the fitness potential of the recipient population. This experiment was conducted during a nonbleaching year, so the potential benefits to recipient population fitness are likely enhanced during bleaching years. In summary, this study demonstrates that outplanting bleaching-resistant corals is a promising tool for elevating the resistance of coral populations to ocean warming.

Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau

Ocean warming and acidification caused by increases of atmospheric carbon dioxide are now thought to be major threats to coral reefs on a global scale. Here we evaluated the environmental conditions and benthic community structures in semi-closed Nikko Bay at the inner reef area in Palau, which has high pCO2 and seawater temperature conditions with high zooxanthellate coral coverage. Nikko Bay is a highly sheltered system with organisms showing low connectivity with surrounding environments, making this bay a unique site for evaluating adaptation and acclimatization responses of organisms to warmed and acidified environments. Seawater pCO2/Ωarag showed strong gradation ranging from 380 to 982 µatm (Ωarag: 1.79–3.66), and benthic coverage, including soft corals and turf algae, changed along with Ωarag while hard coral coverage did not change. In contrast to previous studies, net calcification was maintained in Nikko Bay even under very low mean Ωarag (2.44). Reciprocal transplantation of the dominant coral Porites cylindrica showed that the calcification rate of corals from Nikko Bay did not change when transplanted to a reference site, while calcification of reference site corals decreased when transplanted to Nikko Bay. Corals transplanted out of their origin sites also showed the highest interactive respiration (R) and lower gross photosynthesis (Pg) to respiration (Pg:R), indicating higher energy acquirement of corals at their origin site. The results of this study give important insights about the potential local acclimatization and adaptation capacity of corals to different environmental conditions including pCO2 and temperature.

Potential Local Adaptation of Corals at Acidified and Warmed Nikko Bay, Palau

Ocean warming and acidification caused by the increase of atmospheric carbon dioxide are now thought to be major threats to coral reefs on a global scale. Here we evaluated the environmental conditions and benthic community structures in semi-closed Nikko Bay at the inner reef area in Palau, which has high pCO2 and seawater temperature conditions with high zooxanthellate coral coverage. This bay is a highly sheltered system with organisms showing low connectivity with surrounding environments, making this bay a unique site for evaluating adaptation and acclimatization responses of organisms to warmed and acidified environments. Seawater pCO2/Ωarag showed strong graduation ranging from 380 to 982 µatm (Ωarag: 1.79-3.66) and benthic coverage, including soft corals and turf algae, changed along with Ωarag while hard coral coverage did not. In contrast to previous studies, net calcification was maintained in Nikko Bay even under very low mean Ωarag (2.44). Reciprocal transplantation of the dominant coral Porites cylindrica showed that the calcification rate of corals from Nikko Bay did not change when transplanted to a reference site, while calcification of reference site corals decreased when transplanted to Nikko Bay. Corals transplanted out of their origin sites also showed the highest interactive respiration (R) and lower photosynthesis (P) to respiration (P:R). The results of this study give important insights about the potential local acclimatization and adaptation capacity of corals to different environmental conditions including pCO2 and temperature.

Potential Acclimatization and Adaptive Responses of Adult and Trans-Generation Coral Larvae From a Naturally Acidified Habitat

Coral reefs are one of the most susceptible ecosystems to ocean acidification (OA) caused by increasing atmospheric carbon dioxide (CO2). OA is suspected to impact the calcification rate of corals as well as multiple early life stages including larval and settlement stages. Meanwhile, there is now a strong interest in evaluating if organisms have the potential for acclimatization or adaptation to OA. Here, by taking advantage of a naturally acidified site in Nikko Bay, Palau where corals are presumably exposed to high CO2 conditions for their entire life history, we tested if adult and the next-generation larvae of the brooder coral Pocillopora acuta originating from the high-CO2 site are more tolerant to high CO2 conditions compared to the individuals from a control site. Larvae released from adults collected from the high-CO2 site within the bay and a control site outside the bay were reciprocally cultivated under experimental control or high-CO2 seawater conditions to evaluate their physiology. Additionally, reciprocal transplantation of adult P. acuta corals were conducted between the high-CO2 and control sites in the field. The larvae originating from the control site showed lower Chlorophyll-a content and lipid percentages when reared under high-CO2 compared to control seawater conditions, while larvae originating from the high-CO2 site did not. Additionally, all 10 individuals of adult P. acuta from control site died when transplanted within the bay, while all P. acuta corals within the bay survived at both control and high-CO2 site. Furthermore, P. acuta within the bay showed higher calcification and net photosynthesis rates when exposed to the condition they originated from. These results are one of the first results that indicate the possibility that the long-living corals could enable to show local adaptation to different environmental conditions including high seawater pCO2.

Colonies of Acropora formosa with greater survival potential show conservative calcification rates

Coral reefs are facing increasingly devasting impacts from ocean warming and acidification due to anthropogenic climate change. In addition to reducing greenhouse gas emissions, potential solutions have focused either on reducing light stress during heating, or the potential for identifying or engineering “super corals”. These studies, however, have tended to focus primarily on the bleaching response of corals, and assume that corals that bleach earlier in a thermal event are more likely to die. Here, we explore how survival, potential bleaching, and coral skeletal growth (as branch extension and densification) varies for conspecifics collected from distinctive reef zones at Heron Island on the Southern Great Barrier Reef. A series of reciprocal transplantation experiments were undertaken using the dominant reef building coral (Acropora formosa) between the highly variable ‘reef flat’ and the less variable ‘reef slope’ environments. Coral colonies originating from the reef flat had higher rates of survival and thicker tissues but reduced rates of calcification than conspecifics originating from the reef slope. The energetics of both populations however benefited from greater light intensity offered in the shallows. Reef flat origin corals moved to the lower light intensity of reef slope reduced protein density and calcification rates. For A. formosa, genetic difference, or long-term entrainment to a highly variable environment, appeared to promote coral survival at the expense of calcification. The response divorces coral resilience from carbonate coral reef resilience, a response that was further exacerbated by reductions in irradiance. As we begin to discuss interventions necessitated by the CO2 that has already been released to the atmosphere, we need to prioritise our focus on the properties that maintain valuable carbonate ecosystems. Rapid and dense calcification by corals such as branching Acropora is essential to the ability of carbonate coral reefs to rebound following disturbances events, but may be the first property that is sacrificed to enable coral genet survival under stress.

Bleaching resistant corals retain heat tolerance following acclimatization to environmentally distinct reefs

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine if resistance is retained following transplantation within or beyond a coral’s natal reef. Here we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between environmentally distinct reefs (low vs high diel variability) to determine if stress resistance is retained following transplantation. Critically, transplantation to either environment had no influence on coral bleaching resistance, indicating that this trait was relatively fixed and is thus a useful metric for selecting corals for reef restoration within their native range. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolism was also plastic, with cross transplants of both species matching the performance of native corals at both reefs within three months. Coral physiology (autotrophy, heterotrophy, and metabolism) and overall fitness (survival, growth, and reproduction) were higher at the reef with higher flow and fluctuations in diel pH and dissolved oxygen, and did not differ between native corals and cross-transplants. Conversely, cross-transplants at the low-variability reef had higher fitness than native corals, thus increasing overall fitness of the recipient population. This experiment was conducted during a non-bleaching year, which suggests that introduction of these bleaching-resistant individuals will provide even greater fitness benefits to recipient populations during bleaching years. In summary, this study demonstrates that propagating and transplanting bleaching-resistant corals can elevate the resistance of coral populations to ocean warming while simultaneously maintaining reef function as the climate crisis worsens.

Specificity trumps flexibility—location-based stable associations between Symbiodiniaceae genera and Platygyra verweyi (Scleractinia; Merulinidae)

This study monitored symbiont communities bi-monthly in native coral cores used in a reciprocal transplantation of the coral Platygyra verweyi over two years (2014–2016) and samples of mother colonies from three locations with variable thermal regimes; our results show that associating with multiple Symbiodiniaceae genera (Cladocopium spp. and Durusdinium spp.) is not a prerequisite for symbiont shuffling. Platygyra verweyi associates with certain Symbiodiniaceae genera based on location. Results of quantitative real-time PCR indicated small-scale temporal changes in Symbiodiniaceae genera compositions from 2014 to 2016; however, these changes were not enough to invoke shuffling or switching, despite degree heating weeks exceeding 6 °C-weeks in 2014 and 4 °C-weeks in 2015, which usually resulted in substantial coral bleaching. Microsatellite analysis of the P. verweyi host showed no genetic differences among the study locations. Our results suggest that P. verweyi undergoes long-term acclimatization and/or adaptation based on microgeographic and local environmental conditionsby altering its combinations of associated Symbiodiniaceae. Results also suggest that shuffling might not be as common a phenomenon as it has been given credit for; corals thrive through specific associations, and many corals could still be vulnerable to climate change-induced stress, despite being promiscuous or able to associate with rare and background Symbiodiniaceae genera.