Community-level sensitivity of a calcifying ecosystem to acute in situ CO2 enrichment

The rate of change in ocean carbonate chemistry is a vital determinant in the magnitude of effects observed. Benthic marine ecosystems are facing an increasing risk of acute CO2 exposure that may be natural or anthropogenically derived (e.g. engineering and industrial activities). However, our understanding of how acute CO2 events impact marine life is restricted to individual organisms, with little understanding for how this manifests at the community level. Here, we investigated in situ the effect of acute CO2 enrichment on the coralline algal ecosystem—a globally ubiquitous, ecologically and economically important habitat, but one which is likely to be sensitive to CO2 enrichment due to its highly calcified reef-like structures engineered by coralline algae. Most notably, we observed a rapid community-level shift to favour net dissolution rather than net calcification. Smaller changes from net respiration to net photosynthesis were also observed. There was no effect on the net flux of DMS/DMSP (algal secondary metabolites), nor on the nutrients nitrate and phosphate. Following return to ambient CO2 levels, only a partial recovery was seen within the monitoring timeframe. This study highlights the sensitivity of biogenic carbonate marine communities to acute CO2 enrichment and raises concerns over the capacity for the system to ‘bounce back’ if subjected to repeated acute high-CO2 events

Assessment of Temperature Optimum Signatures of Corals at Both Latitudinal Extremes of the Red Sea

Rising ocean temperatures are pushing reef-building corals beyond their temperature optima (Topt), resulting in reduced physiological performances and increased risk of bleaching. Identifying refugia with thermally resistant corals and understanding their thermal adaptation strategy is therefore urgent to guide conservation actions. The Gulf of Aqaba (GoA, northern Red Sea) is considered a climate refuge, hosting corals that may originate from populations selected for thermal resistance in the warmer waters of the Gulf of Tadjoura (GoT, entrance to the Red Sea and 2000 km south of the GoA). To better understand the thermal adaptation strategy of GoA corals, we compared the temperature optima (Topt) of six common reef-building coral species from the GoA and the GoT by measuring oxygen production and consumption rates as well as photophysiological performance (i.e. chlorophyll fluorescence) in response to a short heat stress. Most species displayed similar Topt between the two locations, highlighting an exceptional continuity in their respective physiological performances across such a large latitudinal range, supporting the GoA refuge theory. Stylophora pistillata showed a significantly lower Topt in the GoA, which may suggest an ongoing population-level selection (i.e. adaptation) to the cooler waters of the GoA and subsequent loss of thermal resistance. Interestingly, all Topt were significantly above the local maximum monthly mean seawater temperatures in the GoA (27.1°C) and close or below in the GoT (30.9°C), indicating that GoA corals, unlike those in the GoT, may survive ocean warming in the next few decades. Finally, Acropora muricata and Porites lobata displayed higher photophysiological performance than most species, which may translate to dominance in local reef communities under future thermal scenarios. Overall, this study is the first to compare the Topt of common reef-building coral species over such a latitudinal range and provides insights into their thermal adaptation in the Red Sea

Standardized Short-Term Acute Heat Stress Assays Resolve Historical Differences in Coral Thermotolerance Across Microhabitat Reef Sites

Coral bleaching is one of the main drivers of reef degradation. Most corals bleach and suffer mortality at just 1–2°C above their maximum monthly mean temperatures, but some species and genotypes resist or recover better than others. Here, we conducted a series of 18‐hr short‐term acute heat stress assays side‐by‐side with a 21‐day long‐term heat stress experiment to assess the ability of both approaches to resolve coral thermotolerance differences reflective of in situ reef temperature thresholds. Using a suite of physiological parameters (photosynthetic efficiency, coral whitening, chlorophyll a , host protein, algal symbiont counts, and algal type association), we assessed bleaching susceptibility of Stylophora pistillata colonies from the windward/exposed and leeward/protected sites of a nearshore coral reef in the central Red Sea, which had previously shown differential mortality during a natural bleaching event. Photosynthetic efficiency was most indicative of the expected higher thermal tolerance in corals from the protected reef site, denoted by an increased retention of dark‐adapted maximum quantum yields at higher temperatures. These differences were resolved using both experimental setups, as corroborated by a positive linear relationship, not observed for the other parameters. Notably, short‐term acute heat stress assays resolved per‐colony (genotype) differences that may have been masked by acclimation effects in the long‐term experiment. Using our newly developed portable experimental system termed the Coral Bleaching Automated Stress System (CBASS), we thus highlight the potential of mobile, standardized short‐term acute heat stress assays to resolve fine‐scale differences in coral thermotolerance. Accordingly, such a system may be suitable for large‐scale determination and complement existing approaches to identify resilient genotypes/reefs for downstream experimental examination and prioritization of reef sites for conservation/restoration. Development of such a framework is consistent with the recommendations of the National Academy of Sciences and the Reef Restoration and Adaptation Program committees for new intervention and restoration strategies

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions

Empirically Derived Thermal Thresholds of Four Coral Species Along the Red Sea Using a Portable and Standardized Experimental Approach

Global warming is causing an unprecedented loss of species and habitats worldwide. This is particularly apparent for tropical coral reefs, with an increasing number of reefs experiencing mass bleaching and mortality on an annual basis. As such, there is a growing need for a standardized experimental approach to rapidly assess the thermal limits of corals and predict the survival of coral species across reefs and regions. Using a portable experimental system, the Coral Bleaching Automated Stress System (CBASS), we conducted standardized 18 h acute thermal stress assays to quantitively determine the upper thermal limits of four coral species across the length of the Red Sea coastline, from the Gulf of Aqaba (GoA) to Djibouti (~ 2100 km). We measured dark-acclimated photosynthetic efficiency (Fv/Fm), algal symbiont density, chlorophyll a, and visual bleaching intensity following heat stress. Fv/Fm was the most precise response variable assessed, advancing the Fv/Fm effective dose 50 (ED50, i.e., the temperature at which 50% of the initial Fv/Fm is measured) as an empirically derived proxy for thermal tolerance. ED50 thermal thresholds from the central/southern Red Sea and Djibouti populations were consistently higher for Acropora hemprichii, Pocillopora verrucosa, and Stylophora pistillata (0.1–1.8 °C above GoA corals, respectively), in line with prevailing warmer maximum monthly means (MMMs), though were lower than GoA corals relative to site MMMs (1.5–3.0 °C). P. verrucosa had the lowest thresholds overall. Despite coming from the hottest site, thresholds were lowest for Porites lobata in the southern Red Sea, suggesting long-term physiological damage or ongoing recovery from a severe, prior bleaching event. Altogether, the CBASS resolved historical, taxonomic, and possibly recent environmental drivers of variation in coral thermal thresholds, highlighting the potential for a standardized, short-term thermal assay as a universal approach for assessing ecological and evolutionary variation in the upper thermal limits of corals

Urbanization comprehensively impairs biological rhythms in coral holobionts

Coral reefs are in global decline due to climate change and anthropogenic influences (Hughes et al., Conservation Biology, 27: 261–269, 2013). Near coastal cities or other densely populated areas, coral reefs face a range of additional challenges. While considerable progress has been made in understanding coral responses to acute individual stressors (Dominoni et al., Nature Ecology & Evolution, 4: 502–511, 2020), the impacts of chronic exposure to varying combinations of sensory pollutants are largely unknown. To investigate the impacts of urban proximity on corals, we conducted a year-long in-natura study—incorporating sampling at diel, monthly, and seasonal time points—in which we compared corals from an urban area to corals from a proximal non-urban area. Here we reveal that despite appearing relatively healthy, natural biorhythms and environmental sensory systems were extensively disturbed in corals from the urban environment. Transcriptomic data indicated poor symbiont performance, disturbance to gametogenic cycles, and loss or shifted seasonality of vital biological processes. Altered seasonality patterns were also observed in the microbiomes of the urban coral population, signifying the impact of urbanization on the holobiont, rather than the coral host alone. These results should raise alarm regarding the largely unknown long-term impacts of sensory pollution on the resilience and survival of coral reefs close to coastal communities

The Coral Bleaching Automated Stress System (CBASS): A low‐cost, portable system for standardized empirical assessments of coral thermal limits

Ocean warming is increasingly affecting marine ecosystems across the globe. Reef-building corals are particularly affected by warming, with mass bleaching events increasing in frequency and leading to widespread coral mortality. Yet, some corals can resist or recover from bleaching better than others. Such variability in thermal resilience could be critical to reef persistence; however, the scientific community lacks standardized diagnostic approaches to rapidly and comparatively assess coral thermal vulnerability prior to bleaching events. We present the Coral Bleaching Automated Stress System (CBASS) as a low-cost, open-source, field-portable experimental system for rapid empirical assessment of coral thermal thresholds using standardized temperature stress profiles and diagnostics. The CBASS consists of four or eight flow-through experimental aquaria with independent water masses, lighting, and individual automated temperature controls capable of delivering custom modulating thermal profiles. The CBASS is used to conduct daily thermal stress exposures that typically include 3-h temperature ramps to multiple target temperatures, a 3-h hold period at the target temperatures, and a 1-h ramp back down to ambient temperature, followed by an overnight recovery period. This mimics shallow water temperature profiles observed in coral reefs and prompts a rapid acute heat stress response that can serve as a diagnostic tool to identify putative thermotolerant corals for in-depth assessments of adaptation mechanisms, targeted conservation, and possible use in restoration efforts. The CBASS is deployable within hours and can assay up to 40 coral fragments/aquaria/day, enabling high-throughput, rapid determination of thermal thresholds for individual genotypes, populations, species, and sites using a standardized experimental framework

The Coral Bleaching Automated Stress System (CBASS): A Low-Cost, Portable System for Standardized Empirical Assessments of Coral Thermal Limits

Ocean warming is increasingly affecting marine ecosystems across the globe. Reef-building corals are particularly affected by warming, with mass bleaching events increasing in frequency and leading to widespread coral mortality. Yet, some corals can resist or recover from bleaching better than others. Such variability in thermal resilience could be critical to reef persistence; however, the scientific community lacks standardized diagnostic approaches to rapidly and comparatively assess coral thermal vulnerability prior to bleaching events. We present the Coral Bleaching Automated Stress System (CBASS) as a low-cost, open-source, field-portable experimental system for rapid empirical assessment of coral thermal thresholds using standardized temperature stress profiles and diagnostics. The CBASS consists of four or eight flow-through experimental aquaria with independent water masses, lighting, and individual automated temperature controls capable of delivering custom modulating thermal profiles. The CBASS is used to conduct daily thermal stress exposures that typically include 3-h temperature ramps to multiple target temperatures, a 3-h hold period at the target temperatures, and a 1-h ramp back down to ambient temperature, followed by an overnight recovery period. This mimics shallow water temperature profiles observed in coral reefs and prompts a rapid acute heat stress response that can serve as a diagnostic tool to identify putative thermotolerant corals for in-depth assessments of adaptation mechanisms, targeted conservation, and possible use in restoration efforts. The CBASS is deployable within hours and can assay up to 40 coral fragments/aquaria/day, enabling high-throughput, rapid determination of thermal thresholds for individual genotypes, populations, species, and sites using a standardized experimental framework

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.Peer reviewe

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 \u3e5℃ 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