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Nature Communications | 2016

Microelectrode characterization of coral daytime interior pH and carbonate chemistry

Wei-Jun Cai; Yuening Ma; Brian M. Hopkinson; Andréa G. Grottoli; M. Warner; Qian Ding; Xinping Hu; Xiangchen Yuan; Verena Schoepf; Hui Xu; Chenhua Han; Todd F. Melman; Kenneth D. Hoadley; D. Tye Pettay; Yohei Matsui; Justin H. Baumann; Stephen Levas; Ye Ying; Yongchen Wang

Reliably predicting how coral calcification may respond to ocean acidification and warming depends on our understanding of coral calcification mechanisms. However, the concentration and speciation of dissolved inorganic carbon (DIC) inside corals remain unclear, as only pH has been measured while a necessary second parameter to constrain carbonate chemistry has been missing. Here we report the first carbonate ion concentration ([CO32−]) measurements together with pH inside corals during the light period. We observe sharp increases in [CO32−] and pH from the gastric cavity to the calcifying fluid, confirming the existence of a proton (H+) pumping mechanism. We also show that corals can achieve a high aragonite saturation state (Ωarag) in the calcifying fluid by elevating pH while at the same time keeping [DIC] low. Such a mechanism may require less H+-pumping and energy for upregulating pH compared with the high [DIC] scenario and thus may allow corals to be more resistant to climate change related stressors.


PLOS ONE | 2013

Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals

Stephen Levas; Andréa G. Grottoli; Adam D. Hughes; Christopher L. Osburn; Yohei Matsui

Mounding corals survive bleaching events in greater numbers than branching corals. However, no study to date has determined the underlying physiological and biogeochemical trait(s) that are responsible for mounding coral holobiont resilience to bleaching. Furthermore, the potential of dissolved organic carbon (DOC) as a source of fixed carbon to bleached corals has never been determined. Here, Porites lobata corals were experimentally bleached for 23 days and then allowed to recover for 0, 1, 5, and 11 months. At each recovery interval a suite of analyses were performed to assess their recovery (photosynthesis, respiration, chlorophyll a, energy reserves, tissue biomass, calcification, δ13C of the skeletal, δ13C, and δ15N of the animal host and endosymbiont fractions). Furthermore, at 0 months of recovery, the assimilation of photosynthetically acquired and zooplankton-feeding acquired carbon into the animal host, endosymbiont, skeleton, and coral-mediated DOC were measured via 13C-pulse-chase labeling. During the first month of recovery, energy reserves and tissue biomass in bleached corals were maintained despite reductions in chlorophyll a, photosynthesis, and the assimilation of photosynthetically fixed carbon. At the same time, P. lobata corals catabolized carbon acquired from zooplankton and seemed to take up DOC as a source of fixed carbon. All variables that were negatively affected by bleaching recovered within 5 to 11 months. Thus, bleaching resilience in the mounding coral P. lobata is driven by its ability to actively catabolize zooplankton-acquired carbon and seemingly utilize DOC as a significant fixed carbon source, facilitating the maintenance of energy reserves and tissue biomass. With the frequency and intensity of bleaching events expected to increase over the next century, coral diversity on future reefs may favor not only mounding morphologies but species like P. lobata, which have the ability to utilize heterotrophic sources of fixed carbon that minimize the impact of bleaching and promote fast recovery.


Proceedings of the Royal Society B: Biological Sciences | 2015

Annual coral bleaching and the long-term recovery capacity of coral

Verena Schoepf; Andréa G. Grottoli; Stephen Levas; Matthew D. Aschaffenburg; Justin H. Baumann; Yohei Matsui; Mark E. Warner

Mass bleaching events are predicted to occur annually later this century. Nevertheless, it remains unknown whether corals will be able to recover between annual bleaching events. Using a combined tank and field experiment, we simulated annual bleaching by exposing three Caribbean coral species (Porites divaricata, Porites astreoides and Orbicella faveolata) to elevated temperatures for 2.5 weeks in 2 consecutive years. The impact of annual bleaching stress on chlorophyll a, energy reserves, calcification, and tissue C and N isotopes was assessed immediately after the second bleaching and after both short- and long-term recovery on the reef (1.5 and 11 months, respectively). While P. divaricata and O. faveolata were able to recover from repeat bleaching within 1 year, P. astreoides experienced cumulative damage that prevented full recovery within this time frame, suggesting that repeat bleaching had diminished its recovery capacity. Specifically, P. astreoides was not able to recover protein and carbohydrate concentrations. As energy reserves promote bleaching resistance, failure to recover from annual bleaching within 1 year will likely result in the future demise of heat-sensitive coral species.


PLOS ONE | 2014

Short-term coral bleaching is not recorded by skeletal boron isotopes

Verena Schoepf; Malcolm T. McCulloch; Mark E. Warner; Stephen Levas; Yohei Matsui; Matthew D. Aschaffenburg; Andréa G. Grottoli

Coral skeletal boron isotopes have been established as a proxy for seawater pH, yet it remains unclear if and how this proxy is affected by seawater temperature. Specifically, it has never been directly tested whether coral bleaching caused by high water temperatures influences coral boron isotopes. Here we report the results from a controlled bleaching experiment conducted on the Caribbean corals Porites divaricata, Porites astreoides, and Orbicella faveolata. Stable boron (δ11B), carbon (δ13C), oxygen (δ18O) isotopes, Sr/Ca, Mg/Ca, U/Ca, and Ba/Ca ratios, as well as chlorophyll a concentrations and calcification rates were measured on coral skeletal material corresponding to the period during and immediately after the elevated temperature treatment and again after 6 weeks of recovery on the reef. We show that under these conditions, coral bleaching did not affect the boron isotopic signature in any coral species tested, despite significant changes in coral physiology. This contradicts published findings from coral cores, where significant decreases in boron isotopes were interpreted as corresponding to times of known mass bleaching events. In contrast, δ13C and δ18O exhibited major enrichment corresponding to decreases in calcification rates associated with bleaching. Sr/Ca of bleached corals did not consistently record the 1.2°C difference in seawater temperature during the bleaching treatment, or alternatively show a consistent increase due to impaired photosynthesis and calcification. Mg/Ca, U/Ca, and Ba/Ca were affected by coral bleaching in some of the coral species, but the observed patterns could not be satisfactorily explained by temperature dependence or changes in coral physiology. This demonstrates that coral boron isotopes do not record short-term bleaching events, and therefore cannot be used as a proxy for past bleaching events. The robustness of coral boron isotopes to changes in coral physiology, however, suggests that reconstruction of seawater pH using boron isotopes should be uncompromised by short-term bleaching events.


PLOS ONE | 2018

Coral physiology and microbiome dynamics under combined warming and ocean acidification

Andréa G. Grottoli; Paula Dalcin Martins; Michael J. Wilkins; Michael D. Johnston; M. Warner; Wei-Jun Cai; Todd F. Melman; Kenneth D. Hoadley; D. Tye Pettay; Stephen Levas; Verena Schoepf; Christian R. Voolstra

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.


Global Change Biology | 2014

The cumulative impact of annual coral bleaching can turn some coral species winners into losers

Andréa G. Grottoli; Mark E. Warner; Stephen Levas; Matthew D. Aschaffenburg; Verena Schoepf; Michael P. McGinley; Justin H. Baumann; Yohei Matsui


Marine Biology | 2016

High-temperature acclimation strategies within the thermally tolerant endosymbiont Symbiodinium trenchii and its coral host, Turbinaria reniformis, differ with changing pCO 2 and nutrients

Kenneth D. Hoadley; D. Tye Pettay; Andréa G. Grottoli; Wei-Jun Cai; Todd F. Melman; Stephen Levas; Verena Schoepf; Qian Ding; Xiangchen Yuan; Yongchen Wang; Yohei Matsui; Justin H. Baumann; Mark E. Warner


Journal of Experimental Marine Biology and Ecology | 2008

Adaptive coloration, behavior and predation vulnerability in three juvenile north Pacific flatfishes

Clifford H. Ryer; Jena L. Lemke; Kate S. Boersma; Stephen Levas


Coral Reefs | 2016

Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals

Stephen Levas; Andréa G. Grottoli; Verena Schoepf; Matthew D. Aschaffenburg; Justin H. Baumann; James E. Bauer; Mark E. Warner


Geochimica et Cosmochimica Acta | 2014

Kinetic and metabolic isotope effects in coral skeletal carbon isotopes: A re-evaluation using experimental coral bleaching as a case study

Verena Schoepf; Stephen Levas; Lisa J. Rodrigues; Michael O. McBride; Matthew D. Aschaffenburg; Yohei Matsui; Mark E. Warner; Adam D. Hughes; Andréa G. Grottoli

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Verena Schoepf

University of Western Australia

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Wei-Jun Cai

University of Delaware

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