Genomic, morphological, and physiological insights into coral acclimation along the depth gradient following an in situ reciprocal transplantation of planulae.

Mesophotic coral reefs have been proposed as refugia for corals, providing shelter and larval propagules for shallow water reefs that are disproportionately challenged by global climate change and local anthropogenic stressors. For mesophotic reefs to be a viable refuge, firstly, deep origin larvae must survive on shallow reefs and, secondly, the two environments must be physically connected. This study tested the first condition. Planulae of the reef-building coral Stylophora pistillata from 5-8 and 40-44 m depth in the Gulf of Aqaba were tested in a long-term reciprocal transplantation experiment for their ability to settle and acclimate to depth in situ. We assessed survival rates, photochemical, physiological, and morphological characteristics in juveniles grown at either their parental origin or transplantation depth. Differences in gene expression patterns were compared between mesophotic and shallow corals at the adult, juvenile, and planula life stages. We found high mortality rates among all mesophotic-origin planulae, irrespective of translocation depth. Gene expression patterns suggested that deep planulae lacked settlement competency and experienced increased developmental stress upon release. For surviving shallow origin juveniles, symbiont photochemical acclimation to depth occurred within 8 days, with symbiont communities showing changes in photochemical traits without algal symbiont shuffling. However, coral host physiological and morphological acclimation towards the typical deep phenotype was incomplete within 60 days. Gene expression was influenced by both life stage and depth. A set of differentially expressed genes (DEGs) associated with initial stress responses following transplantation, latent stress response, and environmental effects of depth was identified. This study therefore refutes the Deep Reef Refugia Hypothesis, as the potential for mesophotic-origin S. pistillata planulae to recruit to the shallow reef is low. The potential remains for shallow planulae to survive at mesophotic depths.

Irradiance driven trophic plasticity in the coral Madracis pharensis from the Eastern Mediterranean.

The distribution of symbiotic scleractinian corals is driven, in part, by light availability, as host energy demands are partially met through translocation of photosynthate. Physiological plasticity in response to environmental conditions, such as light, enables the expansion of resilient phenotypes in the face of changing environmental conditions. Here we compared the physiology, morphology, and taxonomy of the host and endosymbionts of individual Madracis pharensis corals exposed to dramatically different light conditions based on colony orientation on the surface of a shipwreck at 30 m depth in the Bay of Haifa, Israel. We found significant differences in symbiont species consortia, photophysiology, and stable isotopes, suggesting that these corals can adjust multiple aspects of host and symbiont physiology in response to light availability. These results highlight the potential of corals to switch to a predominantly heterotrophic diet when light availability and/or symbiont densities are too low to sustain sufficient photosynthesis, which may provide resilience for corals in the face of climate change.

Insights from the 2-year-long human confinement experiment in Grand Cayman reveal the resilience of coral reef fish communities.

In March 2020, the world went into lockdown to curb the spread of the novel coronavirus (SARS-CoV-2), with immediate impacts on wildlife across ecosystems. The strict 2-year long lockdown in Grand Cayman provided an unprecedented opportunity to assess how the 'human confinement experiment' influenced the community composition of reef fish. Using a suite of multivariate statistics, our findings revealed a stark increase in reef fish biomass during the 2 years of lockdown, especially among herbivores, including parrotfish, with drastic increases in juvenile parrotfishes identified. Additionally, when comparing baseline data of the community from 2018 to the 2 years during lockdown, over a three-fold significant increase in mean reef fish biomass was observed, with a clear shift in community composition. Our findings provide unique insights into the resilience of reef fish communities when local anthropogenic stressors are removed for an unprecedented length of time. Given the functional role of herbivores including parrotfish, our results suggest that reductions in human water-based activities have positive implications for coral reef ecosystems and should be considered in future management strategies.

Morphological and genetic mechanisms underlying the plasticity of the coral Porites astreoides across depths in Bermuda.

The widespread decline of shallow-water coral reefs has fueled interest in assessing whether mesophotic reefs can act as refugia replenishing deteriorated shallower reefs through larval exchange. Here we explore the morphological and molecular basis facilitating survival of planulae and adults of the coral Porites astreoides (Lamarck, 1816; Hexacorallia: Poritidae) along the vertical depth gradient in Bermuda. We found differences in micro-skeletal features such as bigger calyxes and coarser surface of the skeletal spines in shallow corals. Yet, tomographic reconstructions reveal an analogous mineral distribution between shallow and mesophotic adults, pointing to similar skeleton growth dynamics. Our study reveals patterns of host genetic connectivity and minimal symbiont depth-zonation across a broader depth range than previously known for this species in Bermuda. Transcriptional variations across life stages showed different regulation of metabolism and stress response functions, unraveling molecular responses to environmental conditions at different depths. Overall, these findings increase our understanding of coral acclimatory capability across broad vertical gradients, ultimately allowing better evaluation of the refugia potential of mesophotic reefs.

Physiological and morphological plasticity in Stylophora pistillata larvae from Eilat, Israel, to shallow and mesophotic light conditions.

Mesophotic reefs have been proposed as climate change refugia but are not synonymous ecosystems with shallow reefs and remain exposed to anthropogenic impacts. Planulae from the reef-building coral Stylophora pistillata, Gulf of Aqaba, from 5- and 45-m depth were tested ex situ for capacity to settle, grow, and acclimate to reciprocal light conditions. Skeletons were scanned by phase contrast-enhanced micro-CT to study morphology. Deep planulae had reduced volume, smaller diameter on settlement, and greater algal symbiont density. Light conditions did not have significant impact on settlement or mortality rates. Photosynthetic acclimation of algal symbionts was evident within 21-35 days after settlement but growth rate and polyp development were slower for individuals translocated away from their parental origin compared to controls. Though our data reveal rapid symbiont acclimation, reduced growth rates and limited capacity for skeletal modification likely limit the potential for mesophotic larvae to settle on shallow reefs.

Brooded coral offspring physiology depends on the combined effects of parental press and pulse thermal history.

Reef-building corals respond to the temporal integration of both pulse events (i.e., heat waves) and press thermal history (i.e., local environment) via physiological changes, with ecological consequences. We used a "press-pulse-press" experimental framework to expose the brooding coral Porites astreoides to various thermal histories to understand the physiological response of temporal dynamics within and across generations. We collected adult colonies from two reefs (outer Rim reef and inner Patch reef) in Bermuda with naturally contrasting thermal regimes as our initial "press" scenario, followed by a 21-day ex situ "pulse" thermal stress of 30.4°C during larval brooding, and a "press" year-long adult reciprocal transplant between the original sites. Higher endosymbiont density and holobiont protein was found in corals originating from the lower thermal variability site (Rim) compared to the higher thermal variability site (Patch). The thermal pulse event drove significant declines in photosynthesis, endosymbiont density, and chlorophyll a, with bleaching phenotype convergence for adults from both histories. Following the reciprocal transplant, photosynthesis was higher in previously heated corals, indicating recovery from the thermal pulse. The effect of origin (initial press) modulated the response to transplant site for endosymbiont density and chlorophyll a, suggesting contrasting acclimation strategies. Higher respiration and photosynthetic rates were found in corals originating from the Rim site, indicating greater energy available for reproduction, supported by larger larvae released from Rim corals post-transplantation. Notably, parental exposure to the pulse thermal event resulted in increased offspring plasticity when parents were transplanted to foreign sites, highlighting the legacy of the pulse event and the importance of the environment during recovery in contributing to cross-generational or developmental plasticity. Together, these findings provide novel insight into the role of historical disturbance events in driving differential outcomes within and across generations, which is of critical importance in forecasting reef futures.

Physiological characteristics of Stylophora pistillata larvae across a depth gradient.

Depth related parameters, specifically light, affect different aspects of corals physiology, including fluorescence. GFP-like pigments found in many coral species have been suggested to serve a variety of functions, including photo-protection and photo-enhancement. Using fluorescence imaging and molecular analysis, we further investigated the role of these proteins on the physiology of the coral Stylophora pistillata and its algal partners. Fluorescence was found to differ significantly between depths for larvae and adult colonies. Larvae from the shallow reef presented a higher GFP expression and a greater fluorescence intensity compared to the larvae from the mesophotic reef, reflecting the elevated need for photo-protection against high light levels characteristic of the shallow reef, thus supporting the "sunscreen" hypothesis. Additionally, given the lower but still occurring protein expression under non-damaging low light conditions, our results suggest that GFP-like proteins might act to regulate the amount of photosynthetically usable light for the benefit of the symbiotic algae. Moreover, we propose that the differences in GFP expression and green fluorescence between shallow and deep larvae indicate that the GFPs within coral larvae might serve to attract and retain different symbiont clades, increasing the chances of survival when encountering new environments.

Effect of marine antifouling paint particles waste on survival of natural Bermuda copepod communities.

Marine antifouling paints (MAPs) are widely used to prevent organisms from fouling vessel hulls. When scraped from vessels as part of regular maintenance, MAP particles discharged into the seawater become a source of toxic substances, like copper (Cu), to the environment, and biocides leaching from them are known to cause toxic effects on non-target organisms. We investigated the toxicity of MAP particles collected from a Bermuda boatyard on local copepod communities using two experiments. Copepod survival, Chlorophyll a and total dissolved Cu concentrations were measured before and after MAP particles addition. In an acute toxicity test, the addition of 0.3 g/L of MAP particles resulted in 0% copepods survival within 88 h and increased dissolved Cu by 1.8 µM. A significant inverse relationship was observed between copepod survival and MAP particles quantity, highlighting the toxic effects of MAP particles from boat maintenance on copepod communities in the surrounding seawater.

Molecular characterization of nearshore baitfish populations in Bermuda to inform management.

Small-bodied marine fishes play an important role in the food web, feeding both larger fishes and seabirds. Often referred to as baitfishes, they concentrate seasonally in coastal areas in large, often heterospecific assemblages that are targeted by both commercial and recreational fishers. Given apparent declines in at least some of Bermuda's baitfish species over the past 40 years, it is useful to determine the species composition of baitfish assemblages, and how it varies among sites, in order to inform management. Using genetic barcoding of the Cytochrome c oxidase 1 gene (COI), we confirm species identity, assess intraspecific genetic diversity locally, and determine rates of broader genetic connectivity for baitfish assemblages in Bermuda. Species analyzed included Hypoatherina harringtonensis, Anchoa choerostoma, Jenkinsia lamprotaenia, Harengula humeralis, Opisthonema oglinum and Sardinella aurita. Species identification based on molecular barcoding revealed some misidentification of individuals based solely on gross morphological characteristics, with an error rate of 11%, validating the usefulness of this approach. Interestingly, sequence results for the endemic Bermuda anchovy, A. choerostoma, were within 1% similarity to the more broadly distributed big-eye anchovy, A. lamprotaenia, and thus additional analyses are warranted to evaluate the genetic basis for endemism. Estimates of genetic diversity within and among baitfish assemblages in Bermuda were high, indicating high rates of local connectivity among sites for all species. As such, management should consider Bermuda's baitfish species as single, highly mixed populations. However, with the exception of H. humeralis and the endemic A. choerostoma, significant genetic differentiation and population structure were found when comparing Bermuda's baitfish populations with those from other regions, suggesting limited gene flow between other regions and Bermuda for these species. Limited regional connectivity has implications for management, as strong genetic divergence suggests that populations in Bermuda are predominantly self-seeding and thus not likely to be replenished from distant populations. These results therefore support precautionary management of baitfish species in Bermuda.

Do the shuffle: Changes in Symbiodinium consortia throughout juvenile coral development.

Previous studies of symbiotic associations between scleractinians corals and Symbiodinium have demonstrated that the consortium of symbionts can change in response to environmental conditions. However, less is known about symbiont shuffling during early coral development, particularly in brooding species. This study examined whether Symbiodinium consortia (1) varied in Porites astreoides on shallow (10m) and upper mesophotic (30m) reefs, (2) changed during coral development, and (3) influenced growth of juveniles in different environments. Symbiodinium ITS2 sequences were amplified using universal primers and analyzed using phylotype-specific primers designed for phylotypes A, B, and C. Adults from both depths were found to host only phylotype A, phylotypes A and B, or phylotypes A, B, and C and the frequency of the phylotype composition did not vary with depth. However, phylotype A was the dominant symbiont that was vertically transmitted to the planulae. The presence of phylotypes B and C was detected in the majority of juveniles when transplanted onto the shallow and upper mesophotic reefs whereas only phylotype A was detected in the majority of juveniles reared in outdoor aquaria. In addition, growth of juvenile P. astreoides harboring different combinations of Symbiodinium phylotypes did not vary when transplanted to different reef zones. However, juveniles reared in in situ reef environments grew faster than those reared in ex situ outdoor aquaria. These results show that Symbiodinium consortia change during development of P. astreoides and are influenced by environmental conditions.

Population Structure of Montastraea cavernosa on Shallow versus Mesophotic Reefs in Bermuda.

Mesophotic coral reef ecosystems remain largely unexplored with only limited information available on taxonomic composition, abundance and distribution. Yet, mesophotic reefs may serve as potential refugia for shallow-water species and thus understanding biodiversity, ecology and connectivity of deep reef communities is integral for resource management and conservation. The Caribbean coral, Montastraea cavernosa, is considered a depth generalist and is commonly found at mesophotic depths. We surveyed abundance and size-frequency of M. cavernosa populations at six shallow (10m) and six upper mesophotic (45m) sites in Bermuda and found population structure was depth dependent. The mean surface area of colonies at mesophotic sites was significantly smaller than at shallow sites, suggesting that growth rates and maximum colony surface area are limited on mesophotic reefs. Colony density was significantly higher at mesophotic sites, however, resulting in equal contributions to overall percent cover. Size-frequency distributions between shallow and mesophotic sites were also significantly different with populations at mesophotic reefs skewed towards smaller individuals. Overall, the results of this study provide valuable baseline data on population structure, which indicate that the mesophotic reefs of Bermuda support an established population of M. cavernosa.

Toxicity of Deepwater Horizon source oil and the chemical dispersant, Corexit® 9500, to coral larvae.

Acute catastrophic events can cause significant damage to marine environments in a short time period and may have devastating long-term impacts. In April 2010 the BP-operated Deepwater Horizon (DWH) offshore oil rig exploded, releasing an estimated 760 million liters of crude oil into the Gulf of Mexico. This study examines the potential effects of oil spill exposure on coral larvae of the Florida Keys. Larvae of the brooding coral, Porites astreoides, and the broadcast spawning coral, Montastraea faveolata, were exposed to multiple concentrations of BP Horizon source oil (crude, weathered and WAF), oil in combination with the dispersant Corexit® 9500 (CEWAF), and dispersant alone, and analyzed for behavior, settlement, and survival. Settlement and survival of P. astreoides and M. faveolata larvae decreased with increasing concentrations of WAF, CEWAF and Corexit® 9500, however the degree of the response varied by species and solution. P. astreoides larvae experienced decreased settlement and survival following exposure to 0.62 ppm source oil, while M. faveolata larvae were negatively impacted by 0.65, 1.34 and 1.5 ppm, suggesting that P. astreoides larvae may be more tolerant to WAF exposure than M. faveolata larvae. Exposure to medium and high concentrations of CEWAF (4.28/18.56 and 30.99/35.76 ppm) and dispersant Corexit® 9500 (50 and 100 ppm), significantly decreased larval settlement and survival for both species. Furthermore, exposure to Corexit® 9500 resulted in settlement failure and complete larval mortality after exposure to 50 and 100 ppm for M. faveolata and 100 ppm for P. astreoides. These results indicate that exposure of coral larvae to oil spill related contaminants, particularly the dispersant Corexit® 9500, has the potential to negatively impact coral settlement and survival, thereby affecting the resilience and recovery of coral reefs following exposure to oil and dispersants.