Climate, Oxygen, and the Future of Marine Biodiversity.

The ocean enabled the diversification of life on Earth by adding O2 to the atmosphere, yet marine species remain most subject to O2 limitation. Human industrialization is intensifying the aerobic challenges to marine ecosystems by depleting the ocean's O2 inventory through the global addition of heat and local addition of nutrients. Historical observations reveal an ∼2% decline in upper-ocean O2 and accelerating reports of coastal mass mortality events. The dynamic balance of O2 supply and demand provides a unifying framework for understanding these phenomena across scales from the global ocean to individual organisms. Using this framework, we synthesize recent advances in forecasting O2 loss and its impacts on marine biogeography, biodiversity, and biogeochemistry. We also highlight three outstanding uncertainties: how long-term global climate change intensifies ocean weather events in which simultaneous heat and hypoxia create metabolic storms, how differential species O2 sensitivities alter the structure of ecological communities, and how global O2 loss intersects with coastal eutrophication. Projecting these interacting impacts on future marine ecosystems requires integration of climate dynamics, biogeochemistry, physiology, and ecology, evaluated with an eye on Earth history. Reducing global and local impacts of warming and O2 loss will be essential if humankind is to preserve the health and biodiversity of the future ocean.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen 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 outlining 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.

Compound Extreme Events Induce Rapid Mortality in a Tropical Sea Urchin.

AbstractThe frequency, magnitude, and duration of marine heatwaves and deoxygenation events are increasing globally. Recent research suggests that their co-occurrence is more common than previously thought and that their combination can have rapid, dire biological impacts. We used the sea urchin Echinometra lucunter to determine whether mortality occurs faster when deoxygenation events are combined with extreme heating (compound events), compared to deoxygenation events alone. We also tested whether prior exposure to local heatwave conditions accentuates the impacts of compound events. Animals were first exposed for five days to either ambient temperature (28 °C) or a warmer temperature that met the minimum criteria for a local heatwave (30.5 °C). Animals were then exposed to hypoxia, defined as oxygen levels 35% below their average critical oxygen limit, combined with ambient or extreme field temperatures (28 °C, 32 °C). Subsets of animals were removed from the hypoxic treatments every 3 hours for 24 hours to determine how long they could survive. Prior exposure to heatwave conditions did not help or hinder survival under hypoxic conditions, and animals exposed to hypoxia under ambient temperatures experienced little mortality. However, when hypoxia was coupled with extreme temperatures (32 °C), 55% of the animals died within 24 hours. On the reefs at our Panama study site, we found that extreme hypoxic conditions only ever occurred during marine heatwave events, with four compound events occurring in 2018. These results show that short durations (∼1 day) of compound events can be catastrophic and that increases in their duration will severely threaten sea urchin populations.

Spanish AbstractLa frecuencia, magnitud y duración de las olas de calor marinas y los eventos de desoxigenación están aumentando a nivel mundial. Investigaciones recientes sugieren que su coocurrencia es más común de lo que se pensaba anteriormente y que su combinación puede tener impactos biológicos rápidos y nefastos. Usamos el erizo de mar Echinometra lucunter para determinar si la mortalidad de estos ocurre más rápido cuando los eventos de desoxigenación se combinan con un calentamiento extremo (eventos compuestos), en comparación con los eventos de desoxigenación solos. También probamos si la exposición previa a las condiciones locales de olas de calor acentúa los impactos de los eventos compuestos. Primero se expusieron a los animales durante cinco días a temperatura ambiente (28 °C) o una temperatura más cálida que cumpliera con los criterios mínimos para una ola de calor local (30.5 °C). Luego, los animales se expusieron a hipoxia, definida como niveles de oxígeno un 35% por debajo de su límite de oxígeno crítico promedio, combinado con temperaturas ambientales o de campo extremas (28 °C, 32 °C). Se retiraron los subconjuntos de animales de los tratamientos hipóxicos cada 3 horas durante 24 horas para determinar los tiempos de supervivencia. La exposición previa a condiciones de olas de calor no ayudó ni obstaculizó la supervivencia en condiciones hipóxicas, y los animales expuestos a hipoxia en temperatura ambiente experimentaron poca mortalidad. Sin embargo, cuando la hipoxia se combinó con temperaturas extremas (32 °C), el 55% de los animales murió en 24 horas. Las condiciones compuestas en nuestro sitio de estudio en Panamá fueron poco frecuentes y cortas (3 horas). Pero cuando ocurrieron, fueron durante olas de calor marinas, con un total de cuatro eventos compuestos observados en los arrecifes locales durante las olas de calor en 2018. Estos resultados muestran que las duraciones cortas (∼1 día) de eventos compuestos pueden ser catastróficas y aumentar debido al calentamiento, en su duración amenazarán severamente las poblaciones de erizos de mar.

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

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.

Oxygen-mediated plasticity confers hypoxia tolerance in a corallivorous polychaete.

There is mounting evidence that the deoxygenation of coastal marine ecosystems has been underestimated, particularly in the tropics. These physical conditions appear to have far-reaching consequences for marine communities and have been associated with mass mortalities. Yet little is known about hypoxia in tropical habitats or about the effects it has on reef-associated benthic organisms. We explored patterns of dissolved oxygen (DO) throughout Almirante Bay, Panama and found a hypoxic gradient, with areas closest to the mainland having the largest diel variation in DO, as well as more frequent persistent hypoxia. We then designed a laboratory experiment replicating the most extreme in situ DO regime found on shallow patch reefs (3 m) to assess the response of the corallivorous fireworm, Hermodice carnaculata to hypoxia. Worms were exposed to hypoxic conditions (8 hr ~ 1 mg/L or 3.2 kPa) 16 times over an 8-week period, and at 4 and 8 weeks, their oxygen consumption (respiration rates) was measured upon reoxygenation, along with regrowth of severed gills. Exposure to low DO resulted in worms regenerating significantly larger gills compared to worms under normoxia. This response to low DO was coupled with an ability to maintain elevated oxygen consumption/respiration rates after low DO exposure. In contrast, worms from the normoxic treatment had significantly depressed respiration rates after being exposed to low DO (week 8). This indicates that oxygen-mediated plasticity in both gill morphology and physiology may confer tolerance to increasingly frequent and severe hypoxia in one important coral predator associated with reef decline.

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's 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.

An in situ assessment of local adaptation in a calcifying polychaete from a shallow CO2 vent system.

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 is 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 with 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 the low pH site (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 emphasizes the utility of field experiments in natural environments subjected to high level of pCO 2 for elucidating the potential for adaptation to future scenarios of OA.

To brood or not to brood: Are marine invertebrates that protect their offspring more resilient to ocean acidification?

Anthropogenic atmospheric carbon dioxide (CO2) is being absorbed by seawater resulting in increasingly acidic oceans, a process known as ocean acidification (OA). OA is thought to have largely deleterious effects on marine invertebrates, primarily impacting early life stages and consequently, their recruitment and species' survival. Most research in this field has been limited to short-term, single-species and single-life stage studies, making it difficult to determine which taxa will be evolutionarily successful under OA conditions. We circumvent these limitations by relating the dominance and distribution of the known polychaete worm species living in a naturally acidic seawater vent system to their life history strategies. These data are coupled with breeding experiments, showing all dominant species in this natural system exhibit parental care. Our results provide evidence supporting the idea that long-term survival of marine species in acidic conditions is related to life history strategies where eggs are kept in protected maternal environments (brooders) or where larvae have no free swimming phases (direct developers). Our findings are the first to formally validate the hypothesis that species with life history strategies linked to parental care are more protected in an acidifying ocean compared to their relatives employing broadcast spawning and pelagic larval development.