Seawater carbonate chemistry, nutrients and growth rate of coral (Acropora intermedia) and coral-reef seaweed (Lobophora papenfussii) during experiments, 2011

Space competition between corals and seaweeds is an important ecological process underlying coral-reef dynamics. Processes promoting seaweed growth and survival, such as herbivore overfishing and eutrophication, can lead to local reef degradation. Here, we present the case that increasing concentrations of atmospheric CO2 may be an additional process driving a shift from corals to seaweeds on reefs. Coral (Acropora intermedia) mortality in contact with a common coral-reef seaweed (Lobophora papenfussii) increased two- to threefold between background CO2 (400 ppm) and highest level projected for late 21st century (1140 ppm). The strong interaction between CO2 and seaweeds on coral mortality was most likely attributable to a chemical competitive mechanism, as control corals with algal mimics showed no mortality. Our results suggest that coral (Acropora) reefs may become increasingly susceptible to seaweed proliferation under ocean acidification, and processes regulating algal abundance (e.g. herbivory) will play an increasingly important role in maintaining coral abundance.

Diurnal and seasonal measurements of seawater chemistry, temperature and PAR in Hurricane Hole, U.S. Virgin Islands - 2010-2012

Risk analyses indicate that more than 90% of the world's reefs will be threatened by climate change and local anthropogenic impacts by the year 2030 under "business-as-usual" climate scenarios. Increasing temperatures and solar radiation cause coral bleaching that has resulted in extensive coral mortality. Increasing carbon dioxide reduces seawater pH, slows coral growth, and may cause loss of reef structure. Management strategies include establishment of marine protected areas with environmental conditions that promote reef resiliency. However, few resilient reefs have been identified, and resiliency factors are poorly defined. Here we characterize the first natural, non-reef coral refuge from thermal stress and ocean acidification and identify resiliency factors for mangrove-coral habitats. We measured diurnal and seasonal variations in temperature, salinity, photosynthetically active radiation (PAR), and seawater chemistry; characterized substrate parameters; and examined water circulation patterns in mangrove communities where scleractinian corals are growing attached to and under mangrove prop roots in Hurricane Hole, St. John, US Virgin Islands. Additionally, we inventoried the coral species and quantified incidences of coral bleaching, mortality, and recovery for two major reef-building corals, Colpophyllia natans and Diploria labyrinthiformis, growing in mangrove-shaded and exposed (unshaded) areas. Over 30 species of scleractinian corals were growing in association with mangroves. Corals were thriving in low-light (more than 70% attenuation of incident PAR) from mangrove shading and at higher temperatures than nearby reef tract corals. A higher percentage of C. natans colonies were living shaded by mangroves, and no shaded colonies were bleached. Fewer D. labyrinthiformis colonies were shaded by mangroves, however more unshaded colonies were bleached. A combination of substrate and habitat heterogeneity, proximity of different habitat types, hydrographic conditions, and biological influences on seawater chemistry generate chemical conditions that buffer against ocean acidification. This previously undocumented refuge for corals provides evidence for adaptation of coastal organisms and ecosystem transition due to recent climate change. Identifying and protecting other natural, non-reef coral refuges is critical for sustaining corals and other reef species into the future.

Colony-specific calcification and mortality under ocean acidification in the branching coral Montipora digitata

Ocean acidification (OA) threatens calcifying marine organisms including reef-building corals. In this study, we examined the OA responses of individual colonies of the branching scleractinian coral Montipora digitata. We exposed nubbins of unique colonies (n = 15) to ambient or elevated pCO2 under natural light and temperature regimes for 110 days. Although elevated pCO2 exposure on average reduced calcification, individual colonies showed unique responses ranging from declines in positive calcification to negative calcification (decalcification) to no change. Similarly, mortality was greater on average in elevated pCO2, but also showed colony-specific patterns. High variation in colony responses suggests the possibility that ongoing OA may lead to natural selection of OA-tolerant colonies within a coral population.

Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification,warming,and deoxygenation

Changing global climate due to anthropogenic emissions of CO2 are driving rapid changes in the physical and chemical environment of the oceans via warming, deoxygenation, and acidification. These changes may threaten the persistence of species and populations across a range of latitudes and depths, including species that support diverse biological communities that in turn provide ecological stability and support commercial interests. Worldwide, but particularly in the North Atlantic and deep Gulf of Mexico, Lophelia pertusa forms expansive reefs that support biological communities whose diversity rivals that of tropical coral reefs. In this study, L. pertusa colonies were collected from the Viosca Knoll region in the Gulf of Mexico (390 to 450 m depth), genotyped using microsatellite markers, and exposed to a series of treatments testing survivorship responses to acidification, warming, and deoxygenation. All coral nubbins survived the acidification scenarios tested, between pH of 7.67 and 7.90 and aragonite saturation states of 0.92 and 1.47. However, calcification generally declined with respect to pH, though a disparate response was evident where select individuals net calcified and others exhibited net dissolution near a saturation state of 1. Warming and deoxygenation both had negative effects on survivorship, with up to 100% mortality observed at temperatures above 14ºC and oxygen concentrations of approximately 1.5 ml·l-1. These results suggest that, over the short-term, climate change and OA may negatively impact L. pertusa in the Gulf of Mexico, though the potential for acclimation and the effects of genetic background should be considered in future research.

Impacts of food availability and pCO2 on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral Balanophyllia elegans

Ocean acidification, the assimilation of atmospheric CO2 by the oceans that decreases the pH and CaCO3 saturation state (Omega) of seawater, is projected to have severe adverse consequences for calcifying organisms. While strong evidence suggests calcification by tropical reef-building corals containing algal symbionts (zooxanthellae) will decline over the next century, likely responses of azooxanthellate corals to ocean acidification are less well understood. Because azooxanthellate corals do not obtain photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on energy available for calcification. The solitary azooxanthellate orange cup coral Balanophyllia elegans often lives in low-pH, upwelled waters along the California coast. In an 8-month factorial experiment, we measured the effects of three pCO2 treatments (410, 770, and 1220 µatm) and two feeding frequencies (3-day and 21-day intervals) on "planulation" (larval release) by adult B. elegans, and on the survival, skeletal growth, and calcification of newly settled juveniles. Planulation rates were affected by food level but not pCO2. Juvenile mortality was highest under high pCO2 (1220 µatm) and low food (21-day intervals). Feeding rate had a greater impact on calcification of B. elegans than pCO2. While net calcification was positive even at 1220 µatm (~3 times current atmospheric pCO2), overall calcification declined by ~25-45%, and skeletal density declined by ~35-45% as pCO2 increased from 410 to 1220 µatm. Aragonite crystal morphology changed at high pCO2, becoming significantly shorter but not wider at 1220 µatm. We conclude that food abundance is critical for azooxanthellate coral calcification, and that B. elegans may be partially protected from adverse consequences of ocean acidification in habitats with abundant heterotrophic food.

Seawater carbonate chemistry and coral (Acropora digitifera and Acropora tenuis) algal infection rate, survival and surface area of plyps during experiments, 2009

Ocean acidification, caused by increased atmospheric carbon dioxide (CO2) concentrations, is currently an important environmental problem. It is therefore necessary to investigate the effects of ocean acidification on all life stages of a wide range of marine organisms. However, few studies have examined the effects of increased CO2 on early life stages of organisms, including corals. Using a range of pH values (pH 7.3, 7.6, and 8.0) in manipulative duplicate aquarium experiments, we have evaluated the effects of increased CO2 on early life stages (larval and polyp stages) of Acropora spp. with the aim of estimating CO2 tolerance thresholds at these stages. Larval survival rates did not differ significantly between the reduced pH and control conditions. In contrast, polyp growth and algal infection rates were significantly decreased at reduced pH levels compared to control conditions. These results suggest that future ocean acidification may lead to reduced primary polyp growth and delayed establishment of symbiosis. Stress exposure experiments using longer experimental time scales and lower levels of CO2 concentrations than those used in this study are needed to establish the threshold of CO2 emissions required to sustain coral reef ecosystems.

Seawater carbonate chemistry and aerobic performance of coral reef fishes during experiments, 2009

Concerns about the impacts of ocean acidification on marine life have mostly focused on how reduced carbonate saturation affects calcifying organisms. Here, we show that levels of CO2-induced acidification that may be attained by 2100 could also have significant effects on marine organisms by reducing their aerobic capacity. The effects of temperature and acidification on oxygen consumption were tested in 2 species of coral reef fishes, Ostorhinchus doederleini and O. cyanosoma, from the Great Barrier Reef, Australia. The capacity for aerobic activity (aerobic scope) declined at temperatures above the summer average (29°C) and in CO2-acidified water (pH 7.8 and ~1000 ppm CO2) compared to control water (pH 8.15). Aerobic scope declined by 36 and 32% for O. doederleini and O. cyanosoma at temperatures between 29 to 32°C, whereas it declined by 33 and 47% for O. doederleini and O. cyanosoma in acidified water compared to control water. Thus, the declines in aerobic scope in acidified water were similar to those caused by a 3°C increase in water temperature. Minimum aerobic scope values of ~200 mg O2 kg-1 h-1 were attained for both species in acidified water at 32°C, compared with over 600 mg O2 kg-1 h-1 in control water at 29°C. Mortality rate increased sharply at 33°C, indicating that this temperature is close to the lethal thermal limit for both species. Acidification further increased the mortality rate of O. doederleini, but not of O. cyanosoma. These results show that coral reef fishes are sensitive to both higher temperatures and increased levels of dissolved CO2, and that the aerobic performance of some reef fishes could be significantly reduced if climate change continues unabated.

Selective mortality associated with variation in CO2 tolerance in a marine fish

Predicted future CO2 levels can affect reproduction, growth, and behaviour of many marine organisms. However, the capacity of species to adapt to predicted changes in ocean chemistry is largely unknown. We used a unique field-based experiment to test for differential survival associated with variation in CO2 tolerance in a wild population of coral-reef fishes. Juvenile damselfish exhibited variation in their response to elevated (700 µatm) CO2 when tested in the laboratory and this influenced their behaviour and risk of mortality in the wild. Individuals that were sensitive to elevated CO2 were more active and move further from shelter in natural coral reef habitat and, as a result, mortality from predation was significantly higher compared with individuals from the same treatment that were tolerant of elevated CO2. If individual variation in CO2 tolerance is heritable, this selection of phenotypes tolerant to elevated CO2 could potentially help mitigate the effects of ocean acidification.

Seawater carbonate chemistry and length, weight, survival rate, metabolic rate of coral reef fish Amphiprion melanopus in a laboratory experiment

Carbon dioxide concentrations in the surface ocean are increasing owing to rising CO2 concentrations in the atmosphere. Higher CO2 levels are predicted to affect essential physiological processes of many aquatic organisms, leading to widespread impacts on marine diversity and ecosystem function, especially when combined with the effects of global warming. Yet the ability for marine species to adjust to increasing CO2 levels over many generations is an unresolved issue. Here we show that ocean conditions projected for the end of the century (approximately 1,000 µatm CO2 and a temperature rise of 1.5-3.0 °C) cause an increase in metabolic rate and decreases in length, weight, condition and survival of juvenile fish. However, these effects are absent or reversed when parents also experience high CO2 concentrations. Our results show that non-genetic parental effects can dramatically alter the response of marine organisms to increasing CO2 and demonstrate that some species have more capacity to acclimate to ocean acidification than previously thought.

Interactions among chronic and acute impacts on coral recruits: the importance of size-escape thresholds

Newly settled recruits typically suffer high mortality from disturbances, but rapid growth reduces their mortality once size-escape thresholds are attained. Ocean acidification (OA) reduces the growth of recruiting benthic invertebrates, yet no direct effects on survivorship have been demonstrated. We tested whether the reduced growth of coral recruits caused by OA would increase their mortality by prolonging their vulnerability to an acute disturbance: fish herbivory on surrounding algal turf. After two months' growth in ambient or elevated CO2 levels, the linear extension and calcification of coral (Acropora millepora) recruits decreased as CO2 partial pressure (pCO2) increased. When recruits were subjected to incidental fish grazing, their mortality was inversely size dependent. However, we also found an additive effect of pCO2 such that recruit mortality was higher under elevated pCO2 irrespective of size. Compared to ambient conditions, coral recruits needed to double their size at the highest pCO2 to escape incidental grazing mortality. This general trend was observed with three groups of predators (blenny, surgeonfish, and parrotfish), although the magnitude of the fish treatment varied among species. Our study demonstrates the importance of size-escape thresholds in early recruit survival and how OA can shift these thresholds, potentially intensifying population bottlenecks in benthic invertebrate recruitment.

Seawater carbonate chemistry, survival, metamorphosis and respiration rate of coral Acropora digitifera during experiments, 2011

Ocean acidification may negatively impact the early life stages of some marine invertebrates including corals. Although reduced growth of juvenile corals in acidified seawater has been reported, coral larvae have been reported to demonstrate some level of tolerance to reduced pH. We hypothesize that the observed tolerance of coral larvae to low pH may be partly explained by reduced metabolic rates in acidified seawater because both calcifying and non-calcifying marine invertebrates could show metabolic depression under reduced pH in order to enhance their survival. In this study, after 3-d and 7-d exposure to three different pH levels (8.0, 7.6, and 7.3), we found that the oxygen consumption of Acropora digitifera larvae tended to be suppressed with reduced pH, although a statistically significant difference was not observed between pH conditions. Larval metamorphosis was also observed, confirming that successful recruitment is impaired when metamorphosis is disrupted, despite larval survival. Results also showed that the metamorphosis rate significantly decreased under acidified seawater conditions after both short (2 h) and long (7 d) term exposure. These results imply that acidified seawater impacts larval physiology, suggesting that suppressed metabolism and metamorphosis may alter the dispersal potential of larvae and subsequently reduce the resilience of coral communities in the near future as the ocean pH decreases.

Seawater carbonate chemistry, respiration, maximum photochemical efficiency and mortality of brooded larvae of Pocillopora//damicornis in a laboratory experiment

To evaluate the effects of temperature and pCO2 on coral larvae, brooded larvae of Pocillopora damicornis from Nanwan Bay, Taiwan (21°56.179' N, 120°44.85' E), were exposed to ambient (419-470 µatm) and high (604-742 µatm) pCO2 at ~25 and ~29 °C in two experiments conducted in March 2010 and March 2012. Larvae were sampled from four consecutive lunar days (LD) synchronized with spawning following the new moon, incubated in treatments for 24 h, and measured for respiration, maximum photochemical efficiency of PSII (F v/F m), and mortality. The most striking outcome was a strong effect of time (i.e., LD) on larvae performance: respiration was affected by an LD × temperature interaction in 2010 and 2012, as well as an LD × pCO2 × temperature interaction in 2012; F v/F m was affected by LD in 2010 (but not 2012); and mortality was affected by an LD × pCO2 interaction in 2010, and an LD × temperature interaction in 2012. There were no main effects of pCO2 in 2010, but in 2012, high pCO2 depressed metabolic rate and reduced mortality. Therefore, differences in larval performance depended on day of release and resulted in varying susceptibility to future predicted environmental conditions. These results underscore the importance of considering larval brood variation across days when designing experiments. Subtle differences in experimental outcomes between years suggest that transgenerational plasticity in combination with unique histories of exposure to physical conditions can modulate the response of brooded coral larvae to climate change and ocean acidification.

Coral communities exposed to differential large amplitude internal waves cooling and a severe heat stress in 2010 in the Andaman Sea

Tropical scleractinian corals are particularly vulnerable to global warming as elevated sea surface temperatures (SST) disrupt the delicate balance between the coral host and their algal endosymbionts, leading to symbiont expulsion, mass bleaching and mortality. While satellite sensing of SST has proven a good predictor of coral bleaching at the regional scale, there are large deviations in bleaching severity and mortality on the local scale, which are only poorly understood. Here, we show that internal waves play a major role in explaining local coral bleaching and mortality patterns in the Andaman Sea. In spite of a severe region-wide SST anomaly in May 2010, frequent upslope intrusions of cold sub-pycnocline waters due to breaking large amplitude internal waves (LAIW) alleviated heating and mitigated coral bleaching and mortality in shallow LAIW-exposed waters. In LAIW-sheltered waters, by contrast, bleaching susceptible species suffered severe bleaching and total mortality. These findings suggest that LAIW, which are ubiquitous in tropical stratified waters, benefit coral reefs during thermal stress and provide local refugia for bleaching susceptible corals. The swash zones of LAIW may thus be important, so far overlooked, conservation areas for the maintainance of coral diversity in a warming climate. The consideration of LAIW can significantly improve coral bleaching predictions and can provide a valuable tool for coral reef conservation and management.

R-codes, and coral abundance, water temperature and transect characteristics of nearshore reefs in Belize

Coral reefs are increasingly threatened by global and local anthropogenic stressors, such as rising seawater temperature and nutrient enrichment. These two stressors vary widely across the reef face and parsing out their influence on coral communities at reef system scales has been particularly challenging. Here, we investigate the influence of temperature and nutrients on coral community traits and life history strategies on lagoonal reefs across the Belize Mesoamerican Barrier Reef System (MBRS). A novel metric was developed using ultra-high-resolution sea surface temperatures (SST) to classify reefs as enduring low (lowTP), moderate (modTP), or extreme (extTP) temperature parameters over 10 years (2003 to 2012). Chlorophyll-a (chl a) records obtained for the same interval were employed as a proxy for bulk nutrients and these records were complemented with in situ measurements to "sea truth" nutrient content across the three reef types. Chl a concentrations were highest at extTP sites, medial at modTP sites and lowest at lowTP sites. Coral species richness, abundance, diversity, density, and percent cover were lower at extTP sites compared to lowTP and modTP sites, but these reef community traits did not differ between lowTP and modTP sites. Coral life history strategy analyses showed that extTP sites were dominated by hardy stress-tolerant and fast-growing weedy coral species, while lowTP and modTP sites consisted of competitive, generalist, weedy, and stress-tolerant coral species. These results suggest that differences in coral community traits and life history strategies between extTP and lowTP/modTP sites were driven primarily by temperature differences with differences in nutrients across site types playing a lesser role. Dominance of weedy and stress-tolerant genera at extTP sites suggests that corals utilizing these two life history strategies may be better suited to cope with warmer oceans and thus may warrant further protective status during this climate change interval. Data associated with this project are archived here, including: -SST data -Satellite Chl a data -Nutrient measurements -Raw coral community survey data For questions contact Justin Baumann (j.baumann3 gmail.com)

Seawater carbonate chemistry, larval settlement and growth rate during experiments with coral Porites astreoides, 2008

In response to the increases in pCO2 projected in the 21st century, adult coral growth and calcification are expected to decrease significantly. However, no published studies have investigated the effect of elevated pCO2 on earlier life history stages of corals. Porites astreoides larvae were collected from reefs in Key Largo, Florida, USA, settled and reared in controlled saturation state seawater. Three saturation states were obtained, using 1 M HCl additions, corresponding to present (380 ppm) and projected pCO2 scenarios for the years 2065 (560 ppm) and 2100 (720 ppm). The effect of saturation state on settlement and post-settlement growth was evaluated. Saturation state had no significant effect on percent settlement; however, skeletal extension rate was positively correlated with saturation state, with ~50% and 78% reductions in growth at the mid and high pCO2 treatments compared to controls, respectively.