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ABSTRACT Tropical reef ecosystems are strongly influenced by the composition of coral species, but the factors influencing coral diversity and distributions are not fully understood. Here we demonstrate that large variations in the relative abundance of three major coral species across adjacent Caribbean reef sites are strongly related to their different low O₂tolerances. In laboratory experiments designed to mimic reef conditions, the cumulative effect of repeated nightly low O₂drove coral bleaching and mortality, with limited modulation by temperature. After four nights of repeated low O₂, species responses also varied widely, from > 50% bleaching inAcropora cervicornisto no discernable sensitivity ofPorites furcata.A simple metric of hypoxic pressure that combines these experimentally derived species sensitivities with high‐resolution field data accurately predicts the observed relative abundance of species across three reefs. Only the well‐oxygenated reef supported the framework‐building hypoxia‐sensitiveAcropora cervicornis, while the hypoxia‐tolerant weedy speciesPorites furcatawas dominant on the most frequently O₂‐deplete reef. Physiological exclusion of acroporids from these O₂‐deplete reefs underscores the need for hypoxia management to reduce extirpation risk. 

ABSTRACT Global climate change impacts marine ecosystems through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, less is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their tolerance to hypoxia. We conductedin situoxygen manipulations on a coral reef in Bahía Almirante on the Caribbean coast of Panama, which has previously experienced documented episodes of hypoxia. Naïve coral colonies (previously unexposed to hypoxia) ofSiderastrea sidereaandAgaricia lamarckiwere transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress or may represent opportunists exploiting host stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. IMPORTANCEMarine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels aroundSiderastrea sidereaandAgaricia lamarckicoloniesin situto observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress. 

Ocean deoxygenation is intensifying globally due to human activities – and is emerging as a grave threat to coral reef ecosystems where it can cause coral bleaching and mass mortality. However, deoxygenation is one of many threats to coral reefs, making it essential to understand how prior environmental stress may influence responses to deoxygenation. To address this question, we examined responses of the coral holobiont (i.e., the coral host, Symbiodiniaceae, and the microbiome) to deoxygenation in corals with different environmental stress backgrounds. We outplantedAcropora cervicornisfragments of known genotypes from anin situnursery to two sites in the Florida Keys spanning an inshore-offshore gradient. After four months, fragments from the outplanted corals were transferred to the laboratory, where we tested differences in survivorship, tissue loss, photosynthetic efficiency, Symbiodiniaceae cell density, and coral microbiome composition after persistent exposure to one of four oxygen treatments ranging from extreme deoxygenation (0.5 mg L^-1) to normoxia (6 mg L^-1). We found that, for the short duration of exposure tested in this study (four days), the entire coral holobiont was resistant to dissolved oxygen (DO) concentrations as low as 2.0 mg L^-1, but that the responses of members of the holobiont decoupled at 0.5 mg L^-1. In this most extreme treatment, the coral host showed decreased photosynthetic efficiency, tissue loss, and mortality, and lower Symbiodiniaceae densities in a bleaching response, but most microbial taxa remained stable. Although deoxygenation did not cause major community shifts in microbiome composition, the population abundance of some microbial taxa did respond. Site history influenced some responses of the coral host and endosymbiont, but not the coral microbiome, with corals from the more stressful inshore site showing greater susceptibility to subsequent deoxygenation. Our study reveals that coral holobiont members respond differently to deoxygenation, with greater sensitivity in the coral host and Symbiodiniaceae and greater resistance in the coral microbiome, and that prior stress exposure can decrease host tolerance to deoxygenation. 

Abstract. Anthropogenic warming and nutrient over-enrichment of our oceans have resulted in significant, and often catastrophic, reductions in dissolved oxygen (deoxygenation). Stress on water-breathing animals from this deoxygenation has been shown to occur at all levels of biological organization: cellular, organ, individual, species, population, community, and ecosystem. Most climate forecasts predict increases in ocean deoxygenation; thus, it is essential to develop reliable biological indicators of low-oxygen stress that can be used by regional and global oxygen monitoring efforts to detect and assess the impacts of deoxygenation on ocean life. This review focuses on responses to low-oxygen stress that are manifest at different levels of biological organization and at a variety of spatial and temporal scales. We compare particular attributes of these biological indicators to the dissolved oxygen threshold of response, timescales of response, sensitive life stages and taxa, and the ability to scale the response to oxygen stress across levels of organization. Where there is available evidence, we discuss the interactions of other biological and abiotic stressors on the biological indicators of low-oxygen stress. We address the utility, confounding effects, and implementation of the biological indicators of oxygen stress for research and societal applications. Our hope is that further refinement and dissemination of these oxygen stress indicators will provide more direct support for environmental managers, fisheries and mariculture scientists, conservation professionals, and policymakers to confront the challenges of ocean deoxygenation. An improved understanding of the sensitivity of different ocean species, communities, and ecosystems to low-oxygen stress will empower efforts to design monitoring programs, assess ecosystem health, develop management guidelines, track conditions, and detect low-oxygen events.