Highly conserved thermal performance strategies may limit adaptive potential in corals.

Increasing seawater temperatures are expected to have profound consequences for reef-building corals' physiology. Understanding how demography changes in response to chronic exposure to warming will help forecast how coral communities will respond to climate change. Here, we measure growth rates of coral fragments of four common species, while exposing them to temperatures ranging from 19°C to 31°C for one month to calibrate their thermal-performance curves (TPCs). Our results show that, while there are contrasting differences between species, the shape of the TPCs was remarkably consistent among individuals of the same species. The low variation in thermal sensitivity within species may imply a reduced capacity for rapid adaptive responses to future changes in thermal regimes. Additionally, interspecific differences in thermal responses show a negative relationship between maximum growth and thermal optima, contradicting expectations derived from the classic 'warmer-is-better' hypothesis. Among species, there was a trade-off between current and future growth, whereby most species perform well under current thermal regimes but are susceptible to future increases in temperature. Increases in water temperature with climate change are likely to reduce growth rates, further hampering future coral reef recovery rates and potentially altering community composition.

In situ responses of the sponge microbiome to ocean acidification.

Climate change is causing rapid changes in reef structure, biodiversity, and function, though most sponges are predicted to tolerate conditions projected for 2100. Sponges maintain intimate relationships with microbial symbionts, with previous studies suggesting that microbial flexibility may be pivotal to success under ocean acidification (OA). We performed a reciprocal transplantation of the coral reef sponges Coelocarteria singaporensis and Stylissa cf. flabelliformis between a control reef site and an adjacent CO2 vent site in Papua New Guinea to explore how the sponge microbiome responds to OA. Microbial communities of C. singaporensis, which differed initially between sites, did not shift towards characteristic control or vent microbiomes, even though relative abundances of Chloroflexi and Cyanobacteria increased and that of Thaumarchaeota decreased 7 months after transplantation to the control site. Microbial communities of S. cf. flabelliformis, which were initially stable between sites, did not respond specifically to transplantation but collectively exhibited a significant change over time, with a relative increase in Thaumarchaeota and decrease in Proteobacteria in all treatment groups. The lack of a community shift upon transplantation to the vent site suggests that microbial flexibility, at least in the adult life-history stage, does not necessarily underpin host survival under OA .

Ocean acidification alters early successional coral reef communities and their rates of community metabolism.

Ocean acidification is expected to alter community composition on coral reefs, but its effects on reef community metabolism are poorly understood. Here we document how early successional benthic coral reef communities change in situ along gradients of carbon dioxide (CO2), and the consequences of these changes on rates of community photosynthesis, respiration, and light and dark calcification. Ninety standardised benthic communities were grown on PVC tiles deployed at two shallow-water volcanic CO2 seeps and two adjacent control sites in Papua New Guinea. Along the CO2 gradient, both the upward facing phototrophic and the downward facing cryptic communities changed in their composition. Under ambient CO2, both communities were dominated by calcifying algae, but with increasing CO2 they were gradually replaced by non-calcifying algae (predominantly green filamentous algae, cyanobacteria and macroalgae, which increased from ~30% to ~80% cover). Responses were weaker in the invertebrate communities, however ascidians and tube-forming polychaetes declined with increasing CO2. Differences in the carbonate chemistry explained a far greater amount of change in communities than differences between the two reefs and successional changes from five to 13 months, suggesting community successions are established early and are under strong chemical control. As pH declined from 8.0 to 7.8, rates of gross photosynthesis and dark respiration of the 13-month old reef communities (upper and cryptic surfaces combined) significantly increased by 10% and 20%, respectively, in response to altered community composition. As a consequence, net production remained constant. Light and dark calcification rates both gradually declined by 20%, and low or negative daily net calcification rates were observed at an aragonite saturation state of <2.3. The study demonstrates that ocean acidification as predicted for the end of this century will strongly alter reef communities, and will significantly change rates of community metabolism.

Diazotroph diversity and nitrogen fixation in the coral Stylophora pistillata from the Great Barrier Reef.

Diazotrophs, both Bacteria and Archaea, capable of fixing nitrogen (N2), are present in the tissues and mucous, of corals and can supplement the coral holobiont nitrogen budget with fixed nitrogen (N) in the form of ammonia (NH3). Stylophora pistillata from Heron Island on the Great Barrier Reef collected at 5 and 15 m, and experimentally manipulated in the laboratory, showed that the rates of net photosynthesis, steady state quantum yields of photosystem II (PSII) fluorescence (∆Fv/Fm') and calcification varied based on irradiance as expected. Rates of N2 fixation were, however, invariant across treatments while the amount of fixed N contributing to Symbiodinium spp. N demand is irradiance dependent. Additionally, both the Symbiodinium and diazotrophic communities are significantly different based on depth, and novel Cluster V nifH gene phylotypes, which are not known to fix nitrogen, were recovered. A functional analysis using PICRUSt also showed that shallow corals were enriched in genes involved in nitrogen metabolism, and N2 fixation specifically. Corals have evolved a number of strategies to derive nitrogen from organic (e.g., heterotrophic feeding) and inorganic sources (e.g., N2 fixation) to maintain critical pathways such as protein synthesis to succeed ecologically in nitrogen-limited habitats.

Low recruitment due to altered settlement substrata as primary constraint for coral communities under ocean acidification.

The future of coral reefs under increasing CO2 depends on their capacity to recover from disturbances. To predict the recovery potential of coral communities that are fully acclimatized to elevated CO2, we compared the relative success of coral recruitment and later life stages at two volcanic CO2 seeps and adjacent control sites in Papua New Guinea. Our field experiments showed that the effects of ocean acidification (OA) on coral recruitment rates were up to an order of magnitude greater than the effects on the survival and growth of established corals. Settlement rates, recruit and juvenile densities were best predicted by the presence of crustose coralline algae, as opposed to the direct effects of seawater CO2 Offspring from high CO2 acclimatized parents had similarly impaired settlement rates as offspring from control parents. For most coral taxa, field data showed no evidence of cumulative and compounding detrimental effects of high CO2 on successive life stages, and three taxa showed improved adult performance at high CO2 that compensated for their low recruitment rates. Our data suggest that severely declining capacity for reefs to recover, due to altered settlement substrata and reduced coral recruitment, is likely to become a dominant mechanism of how OA will alter coral reefs.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs.

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

Cumulative Effects of Nutrient Enrichment and Elevated Temperature Compromise the Early Life History Stages of the Coral Acropora tenuis.

Inshore coral reefs are experiencing the combined pressures of excess nutrient availability associated with coastal activities and warming seawater temperatures. Both pressures are known to have detrimental effects on the early life history stages of hard corals, but studies of their combined effects on early demographic stages are lacking. We conducted a series of experiments to test the combined effects of nutrient enrichment (three levels) and elevated seawater temperature (up to five levels) on early life history stages of the inshore coral Acropora tenuis, a common species in the Indo-Pacific and Red Sea. Gamete fertilization, larval survivorship and larval settlement were all significantly reduced as temperature increased, but only fertilization was further affected by simultaneous nutrient enrichment. Combined high temperatures and nutrient enrichment affected fertilization in an additive manner, whereas embryo abnormalities increased synergistically. Higher than normal temperatures (32°C) increased coral juvenile growth rates 1.6-fold, but mortality also increased by 50%. The co-occurrence of nutrient enrichment with high temperatures reduced juvenile mortality to 36%, ameliorating temperature stress (antagonistic interaction). Overall, the types of effect (additive vs synergistic or antagonistic) and their magnitude varied among life stages. Gamete and embryo stages were more affected by temperature stress and, in some cases, also by nutrient enrichment than juveniles. The data suggest that coastal runoff events might exacerbate the impacts of warming temperatures on fertilization if these events co-occur during corals spawning. The cumulative impacts of simultaneous exposure to nutrient enrichment and elevated temperatures over all early life history stages increases the likelihood for failure of larval supply and recruitment for this coral species. Our results suggest that improving the water quality of river discharges into coastal areas might help to enhance the thermal tolerances of early life history stages in this common coral species.

Reduced heterotrophy in the stony coral Galaxea fascicularis after life-long exposure to elevated carbon dioxide.

Ocean acidification imposes many physiological, energetic, structural and ecological challenges to stony corals. While some corals may increase autotrophy under ocean acidification, another potential mechanism to alleviate some of the adverse effects on their physiology is to increase heterotrophy. We compared the feeding rates of Galaxea fascicularis colonies that have lived their entire lives under ocean acidification conditions at natural carbon dioxide (CO2) seeps with colonies living under present-day CO2 conditions. When provided with the same quantity and composition of zooplankton as food, corals acclimatized to high CO2 showed 2.8 to 4.8 times depressed rates of zooplankton feeding. Results were consistent over four experiments, from two expeditions and both in field and chamber measurements. Unless replenished by other sources, reduced zooplankton uptake in G. fascicularis acclimatized to ocean acidification is likely to entail a shortage of vital nutrients, potentially jeopardizing their health and survival in future oceans.

Symbiodinium community composition in scleractinian corals is not affected by life-long exposure to elevated carbon dioxide.

Ocean acidification (OA) is expected to negatively affect coral reefs, however little is known about how OA will change the coral-algal symbiosis on which reefs ultimately depend. This study investigated whether there would be differences in coral Symbiodinium types in response to OA, potentially improving coral performance. We used denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region of ribosomal DNA to investigate the dominant types of Symbiodinium associating with six species of scleractinian coral that were exposed to elevated partial pressures of carbon dioxide (pCO2) in situ from settlement and throughout their lives. The study was conducted at three naturally occurring volcanic CO2 seeps (pCO2 ∼500 to 900 ppm, pHTotal 7.8 - 7.9) and adjacent control areas (pCO2 ∼390 ppm, pHTotal ∼8.0 - 8.05) in Papua New Guinea. The Symbiodinium associated with corals living in an extreme seep site (pCO2 >1000 ppm) were also examined. Ten clade C types and three clade D types dominated the 443 coral samples. Symbiodinium types strongly contrasted between coral species, however, no differences were observed due to CO2 exposure. Within five species, 85 - 95% of samples exhibited the same Symbiodinium type across all sites, with remaining rare types having no patterns attributable to CO2 exposure. The sixth species of coral displayed site specific differences in Symbiodinium types, unrelated to CO2 exposure. Symbiodinium types from the coral inhabiting the extreme CO2 seep site were found commonly throughout the moderate seeps and control areas. Our finding that symbiotic associations did not change in response to CO2 exposure suggest that, within the six coral hosts, none of the investigated 13 clade C and D Symbiodinium types had a selective advantage at high pCO2. Acclimatisation through changing symbiotic association therefore does not seem to be an option for Indo-Pacific corals to deal with future OA.