Coral reefs in the Anthropocene Ocean: novel insights from skeletal proxies of climate change, impacts, and resilience

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Oceanography at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2021.Anthropogenic emissions of greenhouse gases are driving rapid changes in ocean conditions. Shallow-water coral reefs are experiencing the brunt of these changes, including intensifying marine heatwaves (MHWs) and rapid ocean acidification (OA). Consequently, coral reefs are in broad-scale decline, threatening the livelihoods of hundreds of millions of people. Ensuring survival of coral reefs in the 21st century will thus require a new management approach that incorporates robust understanding of reef-scale climate change, the mechanisms by which these changes impact corals, and their potential for adaptation. In this thesis, I extract information from within coral skeletons to 1) Quantify the climate changes occurring on coral reefs and the effects on coral growth, 2) Identify differences in the sensitivity of coral reefs to these changes, and 3) Evaluate the adaptation potential of the keystone reef-building coral, Porites. First, I develop a mechanistic Porites growth model and reveal the physicochemical link between OA and skeletal formation. I show that the thickening (densification) of coral skeletal framework is most vulnerable to OA and that, under 21st century climate model projections, OA will reduce Porites skeletal density globally, with greatest impact in the Coral Triangle. Second, I develop an improved metric of thermal stress, and use a skeletal bleaching proxy to quantify coral responses to intensifying heatwaves in the central equatorial Pacific (CEP) since 1982. My work reveals a long history of bleaching in the CEP, and reef-specific differences in thermal tolerance linked to past heatwave exposure implying that, over time, reef communities have adapted to tolerate their unique thermal regimes. Third, I refine the Sr-U paleo-thermometer to enable monthly-resolved sea surface temperatures (SST) generation using laser ablation ICPMS. I show that laser Sr-U accurately captures CEP SST, including the frequency and amplitude of MHWs. Finally, I apply laser Sr-U to reconstruct the past 100 years of SST at Jarvis Island in the CEP, and evaluate my proxy record of bleaching severity in this context. I determine that Porites coral populations on Jarvis Island have not yet adapted to the pace of anthropogenic climate change.This research was supported by US National Science Foundation Awards OCE-1220529, ANT-1246387, OCE-1737311, CE-1601365, OCE-1805618, OCE-1537338, OCE-2016133, and from the Woods Hole Oceanographic Institution through the Ocean Life Institute, the Ocean Ventures Fund, the Grassle Fellowship Fund, and the MIT-WHOI Academic Programs Office. Additional funding was provided by the Taiwan MOST Grant 104-2628-M-001-007-MY3, the Robertson Foundation, the Leverhulme Trust in UK, the Atlantic Donor Advised Fund, The Prince Albert 2 of Monaco Foundation, the Akiko Shiraki Dynner Fund, the New England Aquarium, the Martin Family Society Fellowship for Sustainability, the Gates Millenium Scholarship, the Arthur Vining Davis Foundation, the NOAA Coral Reef Conservation Program, and from the Woods Hole Oceanographic Institution through Investment in Science Fund, the Early Career Award, and the Access to the Sea Award

Ocean acidification has impacted coral growth on the great barrier reef

Author Posting. © American Geophysical Union, 2020. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geophysical Research Letters 47(19), (2020): e2019GL086761, doi:10.1029/2019GL086761.Ocean acidification (OA) reduces the concentration of seawater carbonate ions that stony corals need to produce their calcium carbonate skeletons and is considered a significant threat to the functional integrity of coral reef ecosystems. However, detection and attribution of OA impact on corals in nature are confounded by concurrent environmental changes, including ocean warming. Here we use a numerical model to isolate the effects of OA and temperature and show that OA alone has caused 13 ± 3% decline in the skeletal density of massive Porites corals on the Great Barrier Reef since 1950. This OA‐induced thinning of coral skeletons, also evident in Porites from the South China Sea but not in the central Pacific, reflects enhanced acidification of reef water relative to the surrounding open ocean. Our finding reinforces concerns that even corals that might survive multiple heatwaves are structurally weakened and increasingly vulnerable to the compounding effects of climate change.This work was supported in part by the U.S. National Science Foundation (OCE‐1737311), the Robertson Foundation, the Tiffany & Co. Foundation, the Atlantic Donor Advised Fund, the Investment in Science Fund and The Andrew W. Mellon Foundation Endowed Fund for Innovative Research at the Woods Hole Oceanographic Institution. The data generated in this study are included in the Supporting Information (Data Sets S1–S3) and are also being archived at NOAA National Centers for Environmental Information (NCEI)‐Paleoclimatology Data repository.2021-02-2

Mid-Holocene, coral-based sea surface temperatures in the western tropical Atlantic

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution-NonCommercial‐NoDerivs License. The definitive version was published in Rodriguez, L. G., Cohen, A. L., Ramirez, W., Oppo, D. W., Pourmand, A., Edwards, R. L., Alpert, A. E., & Mollica, N. Mid-Holocene, coral-based sea surface temperatures in the western tropical Atlantic. Paleoceanography and Paleoclimatology, 34(7), (2019): 1234-1245, doi:10.1029/2019PA003571.The Holocene is considered a period of relative climatic stability, but significant proxy data‐model discrepancies exist that preclude consensus regarding the postglacial global temperature trajectory. In particular, a mid‐Holocene Climatic Optimum, ~9,000 to ~5,000 years BP, is evident in Northern Hemisphere marine sediment records, but its absence from model simulations raises key questions about the ability of the models to accurately simulate climate and seasonal biases that may be present in the proxy records. Here we present new mid‐Holocene sea surface temperature (SST) data from the western tropical Atlantic, where twentieth‐century temperature variability and amplitude of warming track the twentieth‐century global ocean. Using a new coral thermometer Sr‐U, we first developed a temporal Sr‐U SST calibration from three modern Atlantic corals and validated the calibration against Sr‐U time series from a fourth modern coral. Two fossil corals from the Enriquillo Valley, Dominican Republic, were screened for diagenesis, U‐series dated to 5,199 ± 26 and 6,427 ± 81 years BP, respectively, and analyzed for Sr/Ca and U/Ca, generating two annually resolved Sr‐U SST records, 27 and 17 years long, respectively. Average SSTs from both corals were significantly cooler than in early instrumental (1870–1920) and late instrumental (1965–2016) periods at this site, by ~0.5 and ~0.75 °C, respectively, a result inconsistent with the extended mid‐Holocene warm period inferred from sediment records. A more complete sampling of Atlantic Holocene corals can resolve this issue with confidence and address questions related to multidecadal and longer‐term variability in Holocene Atlantic climate.This study was supported by NSF OCE 1747746 to Anne Cohen and by NSF OCE 1805618 to Anne Cohen and Delia Oppo. Eric Loss and his crew on Pangaea Exploration's Sea Dragon enabled fieldwork in Martinique, and George P. Lohman, Thomas DeCarlo, and Hanny Rivera assisted with coral coring. Kathryn Pietro and Julia Middleton assisted in the laboratory, and Louis Kerr provided technical support on the SEM at MBL. Gretchen Swarr provided technical support on the Element and iCap ICPMS at WHOI. We also thank Edwin Hernandez, Jose Morales, and Amos Winter for discussion. All data generated in this study will be made publicly available at http://www.ncdc.noaa.gov/data‐ access/paleoclimatology‐data/dataset

The challenges of detecting and attributing ocean acidification impacts on marine ecosystems

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Doo, S. S., Kealoha, A., Andersson, A., Cohen, A. L., Hicks, T. L., Johnson, Z., I., Long, M. H., McElhany, P., Mollica, N., Shamberger, K. E. F., Silbiger, N. J., Takeshita, Y., & Busch, D. S. The challenges of detecting and attributing ocean acidification impacts on marine ecosystems. ICES Journal of Marine Science, 77(7-8), (2020): 2411-2422, https://doi.org/10.1093/icesjms/fsaa094.A substantial body of research now exists demonstrating sensitivities of marine organisms to ocean acidification (OA) in laboratory settings. However, corresponding in situ observations of marine species or ecosystem changes that can be unequivocally attributed to anthropogenic OA are limited. Challenges remain in detecting and attributing OA effects in nature, in part because multiple environmental changes are co-occurring with OA, all of which have the potential to influence marine ecosystem responses. Furthermore, the change in ocean pH since the industrial revolution is small relative to the natural variability within many systems, making it difficult to detect, and in some cases, has yet to cross physiological thresholds. The small number of studies that clearly document OA impacts in nature cannot be interpreted as a lack of larger-scale attributable impacts at the present time or in the future but highlights the need for innovative research approaches and analyses. We summarize the general findings in four relatively well-studied marine groups (seagrasses, pteropods, oysters, and coral reefs) and integrate overarching themes to highlight the challenges involved in detecting and attributing the effects of OA in natural environments. We then discuss four potential strategies to better evaluate and attribute OA impacts on species and ecosystems. First, we highlight the need for work quantifying the anthropogenic input of CO2 in coastal and open-ocean waters to understand how this increase in CO2 interacts with other physical and chemical factors to drive organismal conditions. Second, understanding OA-induced changes in population-level demography, potentially increased sensitivities in certain life stages, and how these effects scale to ecosystem-level processes (e.g. community metabolism) will improve our ability to attribute impacts to OA among co-varying parameters. Third, there is a great need to understand the potential modulation of OA impacts through the interplay of ecology and evolution (eco–evo dynamics). Lastly, further research efforts designed to detect, quantify, and project the effects of OA on marine organisms and ecosystems utilizing a comparative approach with long-term data sets will also provide critical information for informing the management of marine ecosystems.SSD was funded by NSF OCE (grant # 1415268). DSB and PM were supported by the NOAA Ocean Acidification Program and Northwest Fisheries Science Center, MHL was supported by NSF OCE (grant # 1633951), ZIJ was supported by NSF OCE (grant # 1416665) and DOE EERE (grant #DE-EE008518), NJS was supported by NSF OCE (grant # 1924281), ALC was supported by NSF OCE (grant # 1737311), and AA was supported by NSF OCE (grant # 1416518). KEFS, AK, and TLH were supported by Texas A&M University. This is CSUN Marine Biology contribution (# 306)

Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016)

© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Communications Biology 1 (2018): 177, doi:10.1038/s42003-018-0183-7.The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world’s most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015–16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world.Funding for this study was provided by National Science Foundation awards OCE 1537338, OCE 1605365, and OCE 1031971 to A.L.C., and the Robertson Foundation to A.L.C., National Science Foundation Graduate Research Fellowships to T.M.D. and A.E.A., and a National Defense Science and Engineering Graduate Fellowship to H.E.R

Ocean acidification affects coral growth by reducing skeletal density

Ocean acidification (OA) is considered an important threat to coral reef ecosystems, because it reduces the availability of carbonate ions that reef-building corals need to produce their skeletons. However, while theory predicts that coral calcification rates decline as carbonate ion concentrations decrease, this prediction is not consistently borne out in laboratory manipulation experiments or in studies of corals inhabiting naturally low-pH reefs today. The skeletal growth of corals consists of two distinct processes: extension (upward growth) and densification (lateral thickening). Here, we show that skeletal density is directly sensitive to changes in seawater carbonate ion concentration and thus, to OA, whereas extension is not. We present a numerical model of Porites skeletal growth that links skeletal density with the external seawater environment via its influence on the chemistry of coral calcifying fluid. We validate the model using existing coral skeletal datasets from six Porites species collected across five reef sites and use this framework to project the impact of 21st century OA on Porites skeletal density across the global tropics. Our model predicts that OA alone will drive up to 20.3 ± 5.4% decline in the skeletal density of reef-building Porites corals

Ocean Acidification Has Impacted Coral Growth on the Great Barrier Reef

Author Posting. © American Geophysical Union, 2020. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geophysical Research Letters 47(19), (2020): e2019GL086761, doi:10.1029/2019GL086761.Ocean acidification (OA) reduces the concentration of seawater carbonate ions that stony corals need to produce their calcium carbonate skeletons and is considered a significant threat to the functional integrity of coral reef ecosystems. However, detection and attribution of OA impact on corals in nature are confounded by concurrent environmental changes, including ocean warming. Here we use a numerical model to isolate the effects of OA and temperature and show that OA alone has caused 13 ± 3% decline in the skeletal density of massive Porites corals on the Great Barrier Reef since 1950. This OA‐induced thinning of coral skeletons, also evident in Porites from the South China Sea but not in the central Pacific, reflects enhanced acidification of reef water relative to the surrounding open ocean. Our finding reinforces concerns that even corals that might survive multiple heatwaves are structurally weakened and increasingly vulnerable to the compounding effects of climate change.This work was supported in part by the U.S. National Science Foundation (OCE‐1737311), the Robertson Foundation, the Tiffany & Co. Foundation, the Atlantic Donor Advised Fund, the Investment in Science Fund and The Andrew W. Mellon Foundation Endowed Fund for Innovative Research at the Woods Hole Oceanographic Institution. The data generated in this study are included in the Supporting Information (Data Sets S1–S3) and are also being archived at NOAA National Centers for Environmental Information (NCEI)‐Paleoclimatology Data repository.2021-02-2

Repeat bleaching of a central Pacific coral reef over the past six decades (19602016)

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world's most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate