Low and variable ecosystem calcification in a coral reef lagoon under natural acidification

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Limnology and Oceanography 63 (2018): 714–730, doi:10.1002/lno.10662.Laboratory‐based CO2 experiments and studies of naturally low pH coral reef ecosystems reveal negative impacts of ocean acidification on the calcifying communities that build coral reefs. Conversely, in Palau's low pH lagoons, coral cover is high, coral communities are diverse, and calcification rates of two reef‐building corals exhibit no apparent sensitivity to the strong natural gradient in pH and aragonite saturation state (Ωar). We developed two methods to quantify rates of Net Ecosystem Calcification (NEC), the ecosystem‐level balance between calcification and dissolution, in Risong Lagoon, where average daily pH is ∼ 7.9 and Ωar ∼ 2.7. While coral cover in the lagoon is within the range of other Pacific reefs (∼ 26%), NEC rates were among the lowest measured, averaging 25.9 ± 13.7 mmol m−2 d−1 over two 4 d study periods. NEC rates were highly variable, ranging from a low of 13.7 mmol m−2 d−1 in March 2012 to a high of 40.3 mmol m−2 d−1 in November 2013, despite no significant changes in temperature, salinity, inorganic nutrients, Ωar, or pH. Our results indicate that the coral reef community of Risong Lagoon produces just enough calcium carbonate to maintain net positive calcification but comes dangerously close to net zero or negative NEC (net dissolution). Identifying the factors responsible for low NEC rates as well as the drivers of NEC variability in naturally low pH reef systems are key to predicting their futures under 21st century climate change.This work was supported by NSF award 1220529 to A.L.C., S.J.L., and K.E.F.S. and a Woods Hole Oceanographic Institution Postdoctoral Scholarship to K.E.F.S

Observations and a model of net calcification declines in Palau's largest coral reef lagoon between 1992 and 2015

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 Journal of Geophysical Research: Oceans 125(8), (2020): e2020JC016147, doi:10.1029/2020JC016147.Net ecosystem calcification (NEC) rates of Palau's largest lagoon and barrier reef system between 1992 and 2015 are estimated from sparse total alkalinity (TA) and salinity measurements and a tidal exchange model in which surface lagoon water transported offshore on the ebb tide is replaced by saltier (denser) ocean water that sinks to the bottom after entering the lagoon on the flood tide. Observed lagoon salinities are accurately reproduced by the model with no adjustable parameters. To accurately reproduce observed lagoon TA, NEC for the lagoon‐barrier reef system was 70 mmols m−2 day−1 from 1992 to 1998, 35 mmols m−2 day−1 from 1999 to 2012, and 25 mmols m−2 day−1 from 2013 to 2015. This indicates that Palau's largest lagoon and barrier reef system has not recovered, as of 2015, from the 50% decline in NEC in 1998 caused by the loss of coral cover following a severe bleaching event. The cause of the further decline in NEC in 2012–2013 is unclear. Lagoon residence times vary from 8 days during spring tides to 14 days during neap tides and drive substantial spring‐neap variations in lagoon TA (~25% of the mean salinity‐normalized ocean‐lagoon TA difference). Sparse measurements that do not resolve these spring‐neap variations can exhibit apparent long‐term variations in alkalinity that are not due to changes in NEC.This work was partially supported by NSF award 1220529 to A.L.C., S.J.L., and K.E.F.S and NSF award 1737311 to A.L.C. and the Oceanography Department, Texas A&M University K.E.F.S.2021-01-0

Comparison of CO2 dynamics and air-sea exchange in differing tropical reef environments

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Aquatic Geochemistry 19 (2013): 371-397, doi:10.1007/s10498-013-9214-7.Note from corresponding author: authors Feely and Shamberger were added after the initial submission, but before the final submission.An array of MAPCO2 buoys, CRIMP-2, Ala Wai, and Kilo Nalu, deployed in the coastal waters of Hawaii have produced multiyear high temporal resolution CO2 records in three different coral reef environments off the island of Oahu, Hawaii. This study, which includes data from June 2008-December 2011, is part of an integrated effort to understand the factors that influence the dynamics of CO2-carbonic acid system parameters in waters surrounding Pacific high island coral reef ecosystems and subject to differing natural and anthropogenic stresses. The MAPCO2 buoys are located on the Kaneohe Bay backreef, and fringing reef sites on the south shore of O’ahu, Hawai’i. The buoys measure CO2 and O2 in seawater and in the atmosphere at 3-hour intervals, as well as other physical and biogeochemical parameters (CTD, chlorophyll-a, turbidity). The buoy records, combined with data from synoptic spatial sampling, have allowed us to examine the interplay between biological cycles of productivity/respiration and calcification/dissolution and biogeochemical and physical forcings on hourly to inter-annual time scales. Air-sea CO2 gas exchange was also calculated to determine if the locations were sources or sinks of CO2 over seasonal, annual, and interannual time periods. Net annualized fluxes for CRIMP-2, Ala Wai, and Kilo Nalu over the entire study period were 1.15 mol C m-2 yr-1, 0.045 mol C m-2 yr-1, and -0.0056 mol C m-2 yr-1, respectively, where positive values indicate a source or a CO2 flux from the water to the atmosphere, and negative values indicate a sink or flux of CO2 from the atmosphere into the water. These values are of similar magnitude to previous estimates in Kaneohe Bay as well as those reported from other tropical reef environments. Total alkalinity (AT) was measured in conjunction with pCO2 and the carbonic acid system was calculated to compare with other reef systems and open ocean values around Hawaii. These findings emphasize the need for high-resolution data of multiple parameters when attempting to characterize the carbonic-acid system in locations of highly variable physical, chemical, and biological parameters (e.g. coastal systems, reefs).This work was supported in part by a grant/cooperative agreement from the National Oceanic and Atmospheric Administration, Project R/IR-3, which is sponsored by the University of Hawaii Sea Grant College Program, SOEST, under Institutional Grant No. NA09OAR4170060 from NOAA Office of Sea Grant, Department of Commerce.2014-11-0

Coral macrobioerosion is accelerated by ocean acidification and nutrients

Author Posting. © The Author(s), 2014]. This is the author's version of the work. It is posted here by permission of Geological Society of America for personal use, not for redistribution. The definitive version was published in Geology 43 (2015): 7-10, doi: 10.1130/G36147.1.Coral reefs exist in a delicate balance between calcium carbonate (CaCO3) production and CaCO3 loss. Ocean acidification (OA), the CO2-driven decline in seawater pH and CaCO3 saturation state (Ω), threatens to tip this balance by decreasing calcification, and increasing erosion and dissolution. While multiple CO2 manipulation experiments show coral calcification declines under OA, the sensitivity of bioerosion to OA is less well understood. Previous work suggests that coral and coral reef bioerosion increase with decreasing seawater Ω. However, in the surface ocean, Ω and nutrient concentrations often covary, making their relative influence difficult to resolve. Here, we exploit unique natural gradients in Ω and nutrients across the Pacific basin to quantify the impact of these factors, together and independently, on macrobioerosion rates of coral skeletons. Using an automated program to quantify macrobioerosion in 3-D computerized tomography (CT) scans of coral cores, we show that macrobioerosion rates of live Porites colonies in both low-nutrient (oligotrophic) and high-nutrient (>1 µM nitrate) waters increase significantly as Ω decreases. However, the sensitivity of macrobioerosion to Ω is ten times greater under high-nutrient conditions. Our results demonstrate that OA (decreased Ω) alone can increase coral macrobioerosion rates, but the interaction of OA with local stressors exacerbates its impact, accelerating a shift toward net CaCO3 removal from coral reefs.This work was supported by NSF OCE 1041106 to A.L.C. and K.E.S., NSF OCE 1220529 to A.L.C., TNC award PNA/WHOI061810 to A.L.C., NSF Graduate Research Fellowships to T.M.D. and H.C.B., and a WHOI-OLI post-doctoral fellowship to K.E.S.2015-11-1

Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification

Author Posting. © American Geophysical Union, 2017. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research: Oceans 122 (2017): 745–761, doi:10.1002/2016JC012326.Coral reefs are built of calcium carbonate (CaCO3) produced biogenically by a diversity of calcifying plants, animals, and microbes. As the ocean warms and acidifies, there is mounting concern that declining calcification rates could shift coral reef CaCO3 budgets from net accretion to net dissolution. We quantified net ecosystem calcification (NEC) and production (NEP) on Dongsha Atoll, northern South China Sea, over a 2 week period that included a transient bleaching event. Peak daytime pH on the wide, shallow reef flat during the nonbleaching period was ∼8.5, significantly elevated above that of the surrounding open ocean (∼8.0–8.1) as a consequence of daytime NEP (up to 112 mmol C m−2 h−1). Diurnal-averaged NEC was 390 ± 90 mmol CaCO3 m−2 d−1, higher than any other coral reef studied to date despite comparable calcifier cover (25%) and relatively high fleshy algal cover (19%). Coral bleaching linked to elevated temperatures significantly reduced daytime NEP by 29 mmol C m−2 h−1. pH on the reef flat declined by 0.2 units, causing a 40% reduction in NEC in the absence of pH changes in the surrounding open ocean. Our findings highlight the interactive relationship between carbonate chemistry of coral reef ecosystems and ecosystem production and calcification rates, which are in turn impacted by ocean warming. As open-ocean waters bathing coral reefs warm and acidify over the 21st century, the health and composition of reef benthic communities will play a major role in determining on-reef conditions that will in turn dictate the ecosystem response to climate change.NSF Grant Number: 12205292017-07-3

Heterotrophy of oceanic particulate organic matter elevates net ecosystem calcification

Author Posting. © American Geophysical Union, 2019. 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 46(16), (2019): 9851-9860, doi:10.1029/2019GL083726.Coral reef calcification is expected to decline due to climate change stressors such as ocean acidification and warming. Projections of future coral reef health are based on our understanding of the environmental drivers that affect calcification and dissolution. One such driver that may impact coral reef health is heterotrophy of oceanic‐sourced particulate organic matter, but its link to calcification has not been directly investigated in the field. In this study, we estimated net ecosystem calcification and oceanic particulate organic carbon (POCoc) uptake across the Kāne'ohe Bay barrier reef in Hawai'i. We show that higher rates of POCoc uptake correspond to greater net ecosystem calcification rates, even under low aragonite saturation states (Ωar). Hence, reductions in offshore productivity may negatively impact coral reefs by decreasing the food supply required to sustain calcification. Alternatively, coral reefs that receive ample inputs of POCoc may maintain higher calcification rates, despite a global decline in Ωar.Data needed for calculations are available in the supporting information. Additional data can be provided upon request directly from the corresponding author or accessed by links provided in the supporting information. The authors declare no competing financial interests. We thank Texas Sea Grant for providing partial funding for this project to A. Kealoha through the Grants‐In‐Aid of Graduate Research Program. We also thank the NOAA Nancy Foster Scholarship for PhD program funding to A. Kealoha and Texas A&M University for funds awarded to Shamberger that supported this work. This research was also supported by funding from National Science Foundation Grant OCE‐1538628 to Rappé. The Hawaii Institute of Marine Biology (particularly the Rappé Lab and Jason Jones), NOAA's Coral Reef Ecosystem Program, Connie Previti, Serena Smith, and Chris Maupin were instrumental in sample collection and data analysis.2020-02-2

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)

On a Reef Far, Far Away: Anthropogenic Impacts Following Extreme Storms Affect Sponge Health and Bacterial Communities

Terrestrial runoff can negatively impact marine ecosystems through stressors including excess nutrients, freshwater, sediments, and contaminants. Severe storms, which are increasing with global climate change, generate massive inputs of runoff over short timescales (hours to days); such runoff impacted offshore reefs in the northwest Gulf of Mexico (NW GoM) following severe storms in 2016 and 2017. Several weeks after coastal flooding from these events, NW GoM reef corals, sponges, and other benthic invertebrates ∼185 km offshore experienced mortality (2016 only) and/or sub-lethal stress (both years). To assess the impact of storm-derived runoff on reef filter feeders, we characterized the bacterial communities of two sponges, Agelas clathrodes and Xestospongia muta, from offshore reefs during periods of sub-lethal stress and no stress over a three-year period (2016—2018). Sponge-associated and seawater-associated bacterial communities were altered during both flood years. Additionally, we found evidence of wastewater contamination (based on 16S rRNA gene libraries and quantitative PCR) in offshore sponge samples, but not in seawater samples, following these flood years. Signs of wastewater contamination were absent during the no-flood year. We show that flood events from severe storms have the capacity to reach offshore reef ecosystems and impact resident benthic organisms. Such impacts are most readily detected if baseline data on organismal physiology and associated microbiome composition are available. This highlights the need for molecular and microbial time series of benthic organisms in near- and offshore reef ecosystems, and the continued mitigation of stormwater runoff and climate change impacts

Diverse coral communities in naturally acidified waters of a Western Pacific reef

Anthropogenic carbon dioxide emissions are acidifying the oceans, reducing the concentration of carbonate ions ([CO32-) that calcifying organisms need to build and cement coral reefs. To date, studies of a handful of naturally acidified reef systems reveal depauperate communities, sometimes with reduced coral cover and calcification rates, consistent with results of laboratory-based studies. Here we report the existence of highly diverse, coral-dominated reef communities under chronically low pH and aragonite saturation state (Omega ar). Biological and hydrographic processes change the chemistry of the seawater moving across the barrier reefs and into Palau's Rock Island bays, where levels of acidification approach those projected for the western tropical Pacific open ocean by 2100. Nevertheless, coral diversity, cover, and calcification rates are maintained across this natural acidification gradient. Identifying the combination of biological and environmental factors that enable these communities to persist could provide important insights into the future of coral reefs under anthropogenic acidification