Kenneth R. N. Anthony

Ocean acidification causes bleaching and productivity loss in coral reef builders

Ocean acidification represents a key threat to coral reefs by reducing the calcification rate of framework builders. In addition, acidification is likely to affect the relationship between corals and their symbiotic dinoflagellates and the productivity of this association. However, little is known about how acidification impacts on the physiology of reef builders and how acidification interacts with warming. Here, we report on an 8-week study that compared bleaching, productivity, and calcification responses of crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species in response to acidification and warming. Using a 30-tank experimental system, we manipulated CO2 levels to simulate doubling and three- to fourfold increases [Intergovernmental Panel on Climate Change (IPCC) projection categories IV and VI] relative to present-day levels under cool and warm scenarios. Results indicated that high CO2 is a bleaching agent for corals and CCA under high irradiance, acting synergistically with warming to lower thermal bleaching thresholds. We propose that CO2 induces bleaching via its impact on photoprotective mechanisms of the photosystems. Overall, acidification impacted more strongly on bleaching and productivity than on calcification. Interestingly, the intermediate, warm CO2 scenario led to a 30% increase in productivity in Acropora, whereas high CO2 lead to zero productivity in both corals. CCA were most sensitive to acidification, with high CO2 leading to negative productivity and high rates of net dissolution. Our findings suggest that sensitive reef-building species such as CCA may be pushed beyond their thresholds for growth and survival within the next few decades whereas corals will show delayed and mixed responses.

Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity

Suspended particulate matter (SPM) strongly alters the trophic environment of photosymbiotic aquatic organisms. At high particles loads, phototrophic energy gains can be diminished due to light absorption by suspended particles, and stress from particle abrasion or deposition on tissues. However, energy gains are enhanced if organisms are able to use SPM as a food source. For photosymbiotic benthic suspension feeders, increases in SPM concentrations may require both phototrophic and heterotrophic acclimation to sustain a positive energy balance. This study provides an experimental analysis of the effects of contrasting light and SPM regimes on the energy budget (scope for growth) of two zooxanthellate corals (Goniastrea retiformis and Porites cylindrica). Using a factorial design in a flow-through tank system, corals were exposed for 2 months to shaded and unshaded conditions (equivalent to 3-4 m depth at 4 and 16 mg dry weight SPM l(-1), respectively) and a range of controlled SPM loads with a natural organic content ( approximately 3% w/w). In G. retiformis, rates of particle ingestion were a linear function of SPM concentration within a broad range (1-30 mg dry weight l(-1)). After 2 months of shading, photosynthetic acclimation was significant in G. retiformis, but did not compensate for the reduced light level, as daily respiration exceeded daily photosynthesis. However, in response to the prolonged shading, G. retiformis more than doubled its rate of particle feeding. At high SPM treatments (16 mg dw l(-1)), sediment feeding by this species compensated fully for the 35-47% lower phototrophy in the shaded treatment. Due to both photo- and heterotrophic plasticity, G. retiformis gained tissue and skeletal mass at all experimental levels of light and SPM. In contrast, rates of particle intake by P. cylindrica contributed <10% to the energy budget in shaded and <3% in unshaded conditions. Feeding rates of P. cylindrica were half-saturated at approximately 3 mg dry weight l(-1), and four- to eight-fold lower than those of G. retiformis. Skeletal growth was sustained, but tissue mass and lipid contents declined in shaded and high-SPM treatments, and carbon loss due to shading by SPM was not compensated for by particle feeding. Thus, due to a lack of photo- and heterotrophic plasticity, periods of high turbidity resulted in energy deficiency in P. cylindrica, and high turbidity conditions appeared physiologically unsustainable for this species. This study is the first to show heterotrophic plasticity in a symbiotic coral, and to show that such plasticity can offset stress from high particle loads. It demonstrates that changes in the trophic mode of some coral species are a mechanism for sustaining a positive energy balance in turbid environments, thereby broadening their physiological niche.

Ocean acidification and warming will lower coral reef resilience

Ocean warming and acidification from increasing levels of atmospheric CO2 represent major global threats to coral reefs, and are in many regions exacerbated by local-scale disturbances such as overfishing and nutrient enrichment. Our understanding of global threats and local-scale disturbances on reefs is growing, but their relative contribution to reef resilience and vulnerability in the future is unclear. Here, we analyse quantitatively how different combinations of CO2 and fishing pressure on herbivores will affect the ecological resilience of a simplified benthic reef community, as defined by its capacity to maintain and recover to coral-dominated states. We use a dynamic community model integrated with the growth and mortality responses for branching corals (Acropora) and fleshy macroalgae (Lobophora). We operationalize the resilience framework by parameterizing the response function for coral growth (calcification) by ocean acidification and warming, coral bleaching and mortality by warming, macroalgal mortality by herbivore grazing and macroalgal growth via nutrient loading. The model was run for changes in sea surface temperature and water chemistry predicted by the rise in atmospheric CO2 projected from the IPCCs fossil-fuel intensive A1FI scenario during this century. Results demonstrated that severe acidification and warming alone can lower reef resilience (via impairment of coral growth and increased coral mortality) even under high grazing intensity and low nutrients. Further, the threshold at which herbivore overfishing (reduced grazing) leads to a coral–algal phase shift was lowered by acidification and warming. These analyses support two important conclusions: Firstly, reefs already subjected to herbivore overfishing and nutrification are likely to be more vulnerable to increasing CO2. Secondly, under CO2 regimes above 450–500 ppm, management of local-scale disturbances will become critical to keeping reefs within an Acropora-rich domain.

Coral suspension feeding on fine particulate matter

High concentrations of fine suspended particulate matter (SPM) on nearshore coral reefs are generally assumed to be a stress factor for corals. However, the extent to which SPM serves as a food source for corals has not been quantified. Using ¹⁴C-labelled natural particulate matter, this study investigates the relationship between concentration and suspension feeding on fine SPM by four common species of Scleractinian coral on the Great Barrier Reef (GBR), Australia. In ingestion trials, only one species (Porites cylindrica Dana) conformed to traditional saturation-kinetic models (Michaelis–Menten, Hollings type I) with ingestion rates reaching maximum at low to moderate SPM concentrations (4–8 mg l⁻¹). For the remaining three species (Pocillopora damicornis Linnaeus, Montipora digitata Dana and Acropora millepora Ehrenberg) ingestion rates increased linearly over the full range of SPM concentrations (1–30 mg l⁻¹). All study species assimilated a major proportion of the ingested label, but assimilation efficiency was inversely related to SPM concentration. At low concentrations (1 mg l⁻¹), estimates of assimilation efficiency ranged from 89 to 95% of the ingested SPM, decreasing to 40–50% at the highest concentrations (30 mg SPM l⁻¹). The maximum rate of SPM carbon assimilation can cover less than 5% of basic metabolic costs, which is not significantly different from reported contributions of zooplankton feeding to coral energy budgets. More importantly, SPM feeding at high particle concentrations may cover up to half of the carbon and a third of the nitrogen required for tissue growth.

Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia)

Abstract Reef corals occur across a wide range of habitats, from offshore clear waters to nearshore sediment-laden environments. This study tests the hypothesis that corals from turbid nearshore areas have greater capacity to utilise suspended sediment as a food source than conspecifics from less turbid and midshelf areas. The hypothesis was tested on two common and widespread coral species on the Great Barrier Reef (Pocillopora damicornis and Acropora millepora). The particle clearance rates of samples from more turbid reefs were two-fourfold those of conspecifics from less turbid and midshelf reefs. Rates of sediment ingestion were generally a linear function of sediment load indicating no significant saturation within the concentration range of 1–30 mg dry weight l−1. Estimated assimilation efficiency of particulate 14C varied between 50 and 80%, and was maximised for midshelf A. millepora at the lowest sediment concentration, suggesting that heterotrophy is more efficient in oligotrophic habitats. Based on feeding-response curves, assimilation efficiencies, and published records of ambient particle concentrations, representatives of these species on turbid inshore reefs are 10–20 times more heterotrophic on suspended sediment than their conspecifics on less turbid and midshelf reefs.

High CO2 enhances the competitive strength of seaweeds over corals

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.

ReefTemp: An interactive monitoring system for coral bleaching using high‐resolution SST and improved stress predictors

Anomalously high sea surface temperatures (SST) have led to repeated mass coral bleaching events on a global scale. Existing satellite-based systems used to monitor conditions conducive to bleaching are based on low-resolution (0.5°, ∼50 km) SST data. While these systems have served the research and management community well, they have inherent weaknesses that limit their capacity to predict stress on coral reefs at local scales, over which bleaching severity is known to vary dramatically. Here we discuss the development and testing of ReefTemp, a new operational remote sensing application for the Great Barrier Reef that assesses bleaching risk daily using: high-resolution (2 km) SST, regionally validated thermal stress indices, and color-graded legends directly related to past observations of bleaching severity. Given projections of sea temperature rise, ReefTemp is timely as it can accurately predict bleaching severity at a local scale and therefore help to give focus to future research and monitoring efforts.

Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef

Rising anthropogenic CO(2) emissions acidify the oceans, and cause changes to seawater carbon chemistry. Bacterial biofilm communities reflect environmental disturbances and may rapidly respond to ocean acidification. This study investigates community composition and activity responses to experimental ocean acidification in biofilms from the Australian Great Barrier Reef. Natural biofilms grown on glass slides were exposed for 11 d to four controlled pCO(2) concentrations representing the following scenarios: A) pre-industrial (∼300 ppm), B) present-day (∼400 ppm), C) mid century (∼560 ppm) and D) late century (∼1140 ppm). Terminal restriction fragment length polymorphism and clone library analyses of 16S rRNA genes revealed CO(2) -correlated bacterial community shifts between treatments A, B and D. Observed bacterial community shifts were driven by decreases in the relative abundance of Alphaproteobacteria and increases of Flavobacteriales (Bacteroidetes) at increased CO(2) concentrations, indicating pH sensitivity of specific bacterial groups. Elevated pCO(2) (C + D) shifted biofilm algal communities and significantly increased C and N contents, yet O(2) fluxes, measured using in light and dark incubations, remained unchanged. Our findings suggest that bacterial biofilm communities rapidly adapt and reorganize in response to high pCO(2) to maintain activity such as oxygen production.

Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae

Coralline algae are among the most sensitive calcifying organisms to ocean acidification as a result of increased atmospheric carbon dioxide (pCO2). Little is known, however, about the combined impacts of increased pCO2, ocean acidification, and sea surface temperature on tissue mortality and skeletal dissolution of coralline algae. To address this issue, we conducted factorial manipulative experiments of elevated CO2 and temperature and examined the consequences on tissue survival and skeletal dissolution of the crustose coralline alga (CCA) Porolithon (=Hydrolithon) onkodes (Heydr.) Foslie (Corallinaceae, Rhodophyta) on the southern Great Barrier Reef (GBR), Australia. We observed that warming amplified the negative effects of high pCO2 on the health of the algae: rates of advanced partial mortality of CCA increased from <1% to 9% under high CO2 (from 400 to 1,100 ppm) and exacerbated to 15% under warming conditions (from 26°C to 29°C). Furthermore, the effect of pCO2 on skeletal dissolution strongly depended on temperature. Dissolution of P. onkodes only occurred in the high‐pCO2 treatment and was greater in the warm treatment. Enhanced skeletal dissolution was also associated with a significant increase in the abundance of endolithic algae. Our results demonstrate that P. onkodes is particularly sensitive to ocean acidification under warm conditions, suggesting that previous experiments focused on ocean acidification alone have underestimated the impact of future conditions on coralline algae. Given the central role that coralline algae play within coral reefs, these conclusions have serious ramifications for the integrity of coral‐reef ecosystems.

Environmental limits to growth: physiological niche boundaries of corals along turbidity–light gradients

The physiological responses of organisms to resources and environmental conditions are important determinants of niche boundaries. In previous work, functional relationships between organism energetics and environment have been limited to energy intakes. However, energetic costs of maintenance may also depend on the supply of resources. In many mixotrophic organisms, two such resource types are light and particle concentration (turbidity). Using two coral species with contrasting abundances along light and turbidity gradients (Acropora valida and Turbinaria mesenterina), we incorporate the dual resource-stressor roles of these variables by calibrating functional responses of energy costs (respiration and loss of organic carbon) as well as energy intake (photosynthesis and particle feeding). This allows us to characterize physiological niche boundaries along light and turbidity gradients, identify species-specific differences in these boundaries, and assess the sensitivity of these differences to interspecific differences in particular functional response parameters. The turbidity-light niche of T. mesenterina was substantially larger than that of A. valida, consistent with its broader ecological distribution. As expected, the responses of photosynthesis, heterotrophic capacity, respiration, and organic carbon loss to light and turbidity varied between species. Niche boundaries were highly sensitive to the functional responses of energy costs to light and turbidity. Moreover, the study species’ niche differences were almost entirely attributable to species-specific differences in one functional response: that of respiration to turbidity. These results demonstrate that functional responses of energy-loss processes are important determinants of species-specific physiological limits to growth, and thereby of niche differences in reef corals. Given that many resources can stress organisms when supply rates are high, we propose that the functional responses of energy losses will prove to be important determinants of niche differences in other systems as well.