Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Johnson, M. D., Scott, J. J., Leray, M., Lucey, N., Bravo, L. M. R., Wied, W. L., & Altieri, A. H. Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef. Nature Communications, 12(1), (2021): 4522, https://doi.org/10.1038/s41467-021-24777-3.Loss of oxygen in the global ocean is accelerating due to climate change and eutrophication, but how acute deoxygenation events affect tropical marine ecosystems remains poorly understood. Here we integrate analyses of coral reef benthic communities with microbial community sequencing to show how a deoxygenation event rapidly altered benthic community composition and microbial assemblages in a shallow tropical reef ecosystem. Conditions associated with the event precipitated coral bleaching and mass mortality, causing a 50% loss of live coral and a shift in the benthic community that persisted a year later. Conversely, the unique taxonomic and functional profile of hypoxia-associated microbes rapidly reverted to a normoxic assemblage one month after the event. The decoupling of ecological trajectories among these major functional groups following an acute event emphasizes the need to incorporate deoxygenation as an emerging stressor into coral reef research and management plans to combat escalating threats to reef persistence.M.D.J. was funded by postdoctoral fellow awards from the Smithsonian Institution’s Marine Global Earth Observatory (MarineGEO) and the Smithsonian Tropical Research Institute (STRI); M.L. and N.L. were funded by postdoctoral support from the STRI Office of Fellowships. J.J.S. was funded by a grant from the Gordon and Betty Moore Foundation awarded to STRI and UC Davis (doi:10.37807/GBMF5603). L.M.R.B., W.L.W., and A.H.A. were supported by MarineGEO, a private funder, and STRI funds to A.H.A. Many of the computations were conducted on the Smithsonian High-Performance Cluster (SI/HPC), Smithsonian Institution (doi:10.25572/SIHPC). We thank Rachel Collin for facilities support at the Bocas del Toro Research Station, Plinio Gondola and the research station staff for logistical support, Roman Barco for insight into the functional analyses, Sherly Castro for informative feedback, and Mike Fox for assistance with community analyses. Research permits were provided by the Autoridad Nacional del Ambiente de Panamá. This paper is the result of research funded by the National Oceanic and Atmospheric Administration’s National Centers for Coastal Ocean Science Competitive Research Program under award NA18NOS4780170 to A.H.A. and M.D.J. through the University of Florida. This is contribution 257 from the Coastal Hypoxia Research Program and 86 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network

Climate warming erodes tropical reef habitat through frequency and intensity of episodic hypoxia

Climate warming threatens marine life by increasing metabolic oxygen demand while decreasing oxygen availability. Tropical species living in warm, low oxygen environments may be most at risk, but their tolerances and exposures to these stressors remain poorly documented. We evaluated habitat restrictions for two brittle star species from Caribbean coral reefs by integrating field observations, laboratory experiments and an ecophysiological model. The absence of one species from the warmest reefs results from vital activity restrictions during episodic low oxygen extremes, even though average conditions are well within physiological tolerance limits. Over the past decade, warmer temperatures have been significantly correlated with a greater frequency and intensity of hypoxic events. Continued warming will progressively exclude hypoxia-tolerant species, even if average oxygen remains constant. A warming-driven increase in frequency or intensity of low oxygen extremes could similarly accelerate habitat loss across other marine ecosystems. -- Keywords : Oxygen ; Aquatic hypoxia ; Hypoxia ; Coral reefs ; Oxygen metabolism ; Ocean temperature ; Echinoderms ; Climate change

Seawater carbonate chemistry and calcification rate of crustose coralline alga

Prior exposure to variable environmental conditions is predicted to influence the resilience of marine organisms to global change. We conducted complementary 4-month field and laboratory experiments to understand how a dynamic, and sometimes extreme, environment influences growth rates of a tropical reef-building crustose coralline alga and its responses to ocean acidification (OA). Using a reciprocal transplant design, we quantified calcification rates of the Caribbean coralline Lithophyllum sp. at sites with a history of either extreme or moderate oxygen, temperature, and pH regimes. Calcification rates of in situ corallines at the extreme site were 90% lower than those at the moderate site, regardless of origin. Negative effects of corallines originating from the extreme site persisted even after transplanting to more optimal conditions for 20 weeks. In the laboratory, we tested the separate and combined effects of stress and variability by exposing corallines from the same sites to either ambient (Amb: pH 8.04) or acidified (OA: pH 7.70) stable conditions or variable (Var: pH 7.80-8.10) or acidified variable (OA-Var: pH 7.45-7.75) conditions. There was a negative effect of all pH treatments on Lithophyllum sp. calcification rates relative to the control, with lower calcification rates in corallines from the extreme site than from the moderate site in each treatment, indicative of a legacy effect of site origin on subsequent response to laboratory treatment. Our study provides ecologically relevant context to understanding the nuanced effects of OA on crustose coralline algae, and illustrates how local environmental regimes may influence the effects of global change

In-situ seawater pH and temperature during and fitness traits of a calcifying polychaete after a reciprocal transplant experiment in June-July near Ischia, italy

Ocean acidification (OA) is likely to exert selective pressure on natural populations. Our ability to predict which marine species will adapt to OA, and what underlies this adaptive potential, are of high conservation and resource management priority. Using a naturally low pH vent site in the Mediterranean Sea (Castello Aragonese, Ischia) mirroring projected future OA conditions, we carried out a reciprocal transplant experiment to investigate the relative importance of phenotypic plasticity and local adaptation in two populations of the sessile, calcifying polychaete /Simplaria /sp. (Annelida, Serpulidae, Spirorbinae): one residing in low pH and the other from a nearby ambient (i.e. high) pH site. We measured a suite of fitness related traits (i.e. survival, reproductive output, maturation, population growth) and tube growth rates in laboratory-bred F2 generation individuals from both populations reciprocally transplanted back into both ambient and low pH /in situ/ habitats. Both populations showed lower expression in all traits, but increased tube growth rates, when exposed to low pH compared to high pH conditions, regardless of their site of origin suggesting that local adaptation to low pH conditions has not occurred. We also found comparable levels of plasticity in the two populations investigated, suggesting no influence of long-term exposure to low pH on the ability of populations to adjust their phenotype. Despite high variation in trait values among sites and the relatively extreme conditions at sites close to the vents (pH < 7.36), response trends were consistent across traits. Hence, our data suggest that, for /Simplaria /and possibly other calcifiers, neither local adaptations nor sufficient phenotypic plasticity levels appear to suffice in order to compensate for the negative impacts of OA on long-term survival. Our work also underlines the utility of field experiments in natural environments subjected to high level of /p/CO_2 for elucidating the potential for adaptation to future scenarios of OA

Host-associated microbiomes drive structure and function of marine ecosystems

The significance of symbioses between eukaryotic hosts and microbes extends from the organismal to the ecosystem level and underpins the health of Earth\u27s most threatened marine ecosystems. Despite rapid growth in research on host-associated microbes, from individual microbial symbionts to host-associated consortia of significantly relevant taxa, little is known about their interactions with the vast majority of marine host species. We outline research priorities to strengthen our current knowledge of host-microbiome interactions and how they shape marine ecosystems. We argue that such advances in research will help predict responses of species, communities, and ecosystems to stressors driven by human activity and inform future management strategies

Integrative approaches to understanding organismal responses to aquatic deoxygenation

Oxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two—warming and acidification— that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume (“An Oxygen Perspective on Climate Change”), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by out-lining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects