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.

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.

Selection of mesophotic habitats by Oculina patagonica in the Eastern Mediterranean Sea following global warming.

Globally, species are migrating in an attempt to track optimal isotherms as climate change increasingly warms existing habitats. Stony corals are severely threatened by anthropogenic warming, which has resulted in repeated mass bleaching and mortality events. Since corals are sessile as adults and with a relatively old age of sexual maturity, they are slow to latitudinally migrate, but corals may also migrate vertically to deeper, cooler reefs. Herein we describe vertical migration of the Mediterranean coral Oculina patagonica from less than 10 m depth to > 30 m. We suggest that this range shift is a response to rapidly warming sea surface temperatures on the Israeli Mediterranean coastline. In contrast to the vast latitudinal distance required to track temperature change, this species has migrated deeper where summer water temperatures are up to 2 °C cooler. Comparisons of physiology, morphology, trophic position, symbiont type, and photochemistry between deep and shallow conspecifics revealed only a few depth-specific differences. At this study site, shallow colonies typically inhabit low light environments (caves, crevices) and have a facultative relationship with photosymbionts. We suggest that this existing phenotype aided colonization of the mesophotic zone. This observation highlights the potential for other marine species to vertically migrate.

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance.

Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5℃ above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during recolonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus central Red Sea (CRS) Stylophora pistillata corals using multi-temperature acute thermal stress assays to determine thermal thresholds. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7℃ above MMM). However, absolute thermal thresholds of CRS corals were on average 3℃ above those of GoA corals. To explore the molecular underpinnings, we determined gene expression and microbiome response of the coral holobiont. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals and their symbiotic algae versus a remarkably muted response in CRS colonies. Concomitant to this, coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression (front-loading) in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed stable assemblages. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that may affect the response of coral populations to ocean warming.

Warming resistant corals from the Gulf of Aqaba live close to their cold-water bleaching threshold.

Global climate change is causing increasing variability and extremes in weather worldwide, a trend set to continue. In recent decades both anomalously warm and cold seawater temperatures have resulted in mass coral bleaching events. Whilst corals' response to elevated temperature has justifiably attracted substantial research interest, coral physiology under cold water stress is relatively unfamiliar. The response to below typical winter water temperature was tested for two common reef building species from the Gulf of Aqaba in an ex situ experiment. Stylophora pistillata and Acropora eurystoma were exposed to 1 or 3 °C below average winter temperature and a suite of physiological parameters were assessed. At 3 °C below winter minima (ca. 18.6 °C), both species had significant declines in photosynthetic indices (maximum quantum yield, electron transport rate, saturation irradiance, and photochemical efficiency) and chlorophyll concentration compared to corals at ambient winter temperatures. It was previously unknown that corals at this site live close to their cold-water bleaching threshold and may be vulnerable as climate variability increases in magnitude. In order to determine if a cold winter reduces the known heat resistance of this population, the corals were subsequently exposed to an acute warm period at 30 °C the following summer. Exposed to above typical summer temperatures, both species showed fewer physiological deviations compared to the cold-water stress. Therefore, the cold winter experience did not increase corals' susceptibility to above ambient summer temperatures. This study provides further support for the selection of heat tolerant genotypes colonising the Red Sea basin and thereby support the mechanism behind the Reef Refuge Hypothesis.

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata.

Successful reproductive output and recruitment is crucial to coral persistence and recovery following anthropogenic stress. Feeding is known to alter coral physiology and increase resilience to bleaching.The goal of the study was to address the knowledge gap of the influence of feeding on reproductive output and offspring phenotype.Colonies of Stylophora pistillata from the Northern Gulf of Aqaba (Red Sea) were fed an Artemia diet or unfed for 5 months during gametogenesis, fertilization, and brooding. In addition, time to settlement and mortality of planulae were assessed at water temperatures ranging from winter temperature (22°C) to three degrees above average peak summer temperature (31°C). A range of physiological parameters was measured in parents and offspring.In brooding parents, feeding significantly increased protein concentration and more than tripled the number of released planulae. Planulae from unfed colonies had higher chlorophyll per symbiont concentration and concomitantly higher photosynthetic efficiency compared to planulae from fed parents. In settlement assays, planulae showed a similar thermal resistance as known for this Red Sea adult population. Mortality was greater in planulae from unfed parents at ambient and 3°C above ambient temperature despite higher per offspring investment in terms of total fatty acid content. Fatty acid profiles and relative abundances were generally conserved between different fed and unfed colonies but planulae were enriched in monounsaturated fatty acids relative to adults, that is, 16:1, 18:1, 20:1, 22:1, and 24:1 isomers.Ultimately the availability of zooplankton could influence population physiology and recruitment in corals.

Developmental carryover effects of ocean warming and acidification in corals from a potential climate refugium, the Gulf of Aqaba.

Coral reefs are degrading from the effects of anthropogenic activities, including climate change. Under these stressors, their ability to survive depends upon existing phenotypic plasticity, but also transgenerational adaptation. Parental effects are ubiquitous in nature, yet empirical studies of these effects in corals are scarce, particularly in the context of climate change. This study exposed mature colonies of the common reef-building coral Stylophora pistillata from the Gulf of Aqaba to seawater conditions likely to occur just beyond the end of this century during the peak planulae brooding season (Representative Concentration Pathway 8.5: pH -0.4 and +5°C beyond present day). Parent and planulae physiology were assessed at multiple time points during the experimental incubation. After 5 weeks of incubation, the physiology of the parent colonies exhibited limited treatment-induced changes. All significant time-dependent changes in physiology occurred in both ambient and treatment conditions. Planulae were also resistant to future ocean conditions, with protein content, symbiont density, photochemistry, survival and settlement success not significantly different compared with under ambient conditions. High variability in offspring physiology was independent of parental or offspring treatments and indicate the use of a bet-hedging strategy in this population. This study thus demonstrates weak climate-change-associated carryover effects. Furthermore, planulae display temperature and pH resistance similar to those of adult colonies and therefore do not represent a larger future population size bottleneck. The findings add support to the emerging hypothesis that the Gulf of Aqaba may serve as a coral climate change refugium aided by these corals' inherent broad physiological resistance.

Eutrophication may compromise the resilience of the Red Sea coral Stylophora pistillata to global change.

Environmental stressors are adversely affecting coral reef ecosystems. There is ample evidence that scleractinian coral growth and physiology may be compromised by reduced pH, and elevated temperature, and that this is exacerbated by local environmental stressors. The Gulf of Aqaba is considered a coral reef refuge from acidification and warming but coastal development and nutrient effluent may pose a local threat. This study examined the effects of select forecasted environmental changes (acidification, warming, and increased nutrients) individually and in combination on the coral holobiont Stylophora pistillata from the Gulf of Aqaba to understand how corals in a potential global climate change refugia may fare in the face of local eutrophication. The results indicate interactions between all stressors, with elevated nutrient concentrations having the broadest individual and additive impacts upon the performance of S. pistillata. These findings highlight the importance of maintaining oligotrophic conditions to secure these reefs as potential refugia.

Enhanced transfer of organic matter to higher trophic levels caused by ocean acidification and its implications for export production: A mass balance approach.

Ongoing acidification of the ocean through uptake of anthropogenic CO2 is known to affect marine biota and ecosystems with largely unknown consequences for marine food webs. Changes in food web structure have the potential to alter trophic transfer, partitioning, and biogeochemical cycling of elements in the ocean. Here we investigated the impact of realistic end-of-the-century CO2 concentrations on the development and partitioning of the carbon, nitrogen, phosphorus, and silica pools in a coastal pelagic ecosystem (Gullmar Fjord, Sweden). We covered the entire winter-to-summer plankton succession (100 days) in two sets of five pelagic mesocosms, with one set being CO2 enriched (~760 µatm pCO2) and the other one left at ambient CO2 concentrations. Elemental mass balances were calculated and we highlight important challenges and uncertainties we have faced in the closed mesocosm system. Our key observations under high CO2 were: (1) A significantly amplified transfer of carbon, nitrogen, and phosphorus from primary producers to higher trophic levels, during times of regenerated primary production. (2) A prolonged retention of all three elements in the pelagic food web that significantly reduced nitrogen and phosphorus sedimentation by about 11 and 9%, respectively. (3) A positive trend in carbon fixation (relative to nitrogen) that appeared in the particulate matter pool as well as the downward particle flux. This excess carbon counteracted a potential reduction in carbon sedimentation that could have been expected from patterns of nitrogen and phosphorus fluxes. Our findings highlight the potential for ocean acidification to alter partitioning and cycling of carbon and nutrients in the surface ocean but also show that impacts are temporarily variable and likely depending upon the structure of the plankton food web.

Abundance of the iron containing biomolecule, heme b, during the progression of a spring phytoplankton bloom in a mesocosm experiment.

Concentrations of heme b were determined in a mesocosm experiment situated in Gullmar Fjord off Sweden. The mesocosm experiment lasted for ca. one hundred days and was characterised by the growth of a primary nutrient replete and a secondary nutrient deplete phytoplankton bloom. Heme b varied between 40 ± 10 pmol L-1 in the prebloom period up to a maximum of 700 ± 400 pmol L-1 just prior to the time of the primary chlorophyll a maximum. Thereafter, heme b concentrations decreased again to an average of 120 ± 60 pmol L-1. When normalised to total particulate carbon, heme b was most abundant during the initiation of the nutrient replete spring bloom, when ratios reached 52 ± 24 µmol mol-1; ten times higher than values observed both pre and post the primary bloom. Concentrations of heme b correlated with those of chlorophyll a. Nevertheless, differences were observed in the relative concentrations of the two parameters, with heme b concentrations increasing relative to chlorophyll a during the growth of the primary bloom, decreasing over the period of the secondary bloom and increasing again through the latter period of the experiment. Heme b abundance was therefore influenced by nutrient concentrations and also likely by changing community composition. In half of the mesocosms, pCO2 was elevated and maintained at ca.1000 µatm, however we observed no significant differences between heme b in plus or ambient pCO2 mesocosms, either in absolute terms, or relative to total particulate carbon and chlorophyll a. The results obtained in this study contribute to our understanding of the distribution of this significant component of the biogenic iron pool, and provide an iron replete coastal water end member that aids the interpretation of the distributions of heme b in more iron deplete open ocean waters.

Influence of Ocean Acidification on a Natural Winter-to-Summer Plankton Succession: First Insights from a Long-Term Mesocosm Study Draw Attention to Periods of Low Nutrient Concentrations.

Every year, the oceans absorb about 30% of anthropogenic carbon dioxide (CO2) leading to a re-equilibration of the marine carbonate system and decreasing seawater pH. Today, there is increasing awareness that these changes-summarized by the term ocean acidification (OA)-could differentially affect the competitive ability of marine organisms, thereby provoking a restructuring of marine ecosystems and biogeochemical element cycles. In winter 2013, we deployed ten pelagic mesocosms in the Gullmar Fjord at the Swedish west coast in order to study the effect of OA on plankton ecology and biogeochemistry under close to natural conditions. Five of the ten mesocosms were left unperturbed and served as controls (~380 µatm pCO2), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (~760 µatm pCO2). We ran the experiment for 113 days which allowed us to study the influence of high CO2 on an entire winter-to-summer plankton succession and to investigate the potential of some plankton organisms for evolutionary adaptation to OA in their natural environment. This paper is the first in a PLOS collection and provides a detailed overview on the experimental design, important events, and the key complexities of such a "long-term mesocosm" approach. Furthermore, we analyzed whether simulated end-of-the-century carbonate chemistry conditions could lead to a significant restructuring of the plankton community in the course of the succession. At the level of detail analyzed in this overview paper we found that CO2-induced differences in plankton community composition were non-detectable during most of the succession except for a period where a phytoplankton bloom was fueled by remineralized nutrients. These results indicate: (1) Long-term studies with pelagic ecosystems are necessary to uncover OA-sensitive stages of succession. (2) Plankton communities fueled by regenerated nutrients may be more responsive to changing carbonate chemistry than those having access to high inorganic nutrient concentrations and may deserve particular attention in future studies.