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Species-Specific Responses to Climate Change and Community Composition Determine Future Calcification Rates of Florida Keys Reefs

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Species-Specific Responses to Climate Change and Community Composition Determine Future Calcification Rates of Florida Keys Reefs Growth responses of Caribbean coral species Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs Remy R. Okazaki*1,2,3, Erica K. Towle1, Ruben van Hooidonk4, Carolina Mor1, Rivah N. Winter1, Alan M. Piggot5, Ross Cunning1, Andrew C. Baker1, James S. Klaus6, Peter K. Swart5, Chris Langdon1 1- Department of Marine Biology and Ecology, University of Miami Rosenstiel School of Marine and Atmospheric Science 4600 Rickenbacker Cswy, Miami, FL 33149, USA 2- University of Washington, Joint Institute for the Study of the Atmosphere and Ocean 3737 Brooklyn Ave NE, Seattle, WA 98195, USA 3- NOAA Pacific Marine Environmental Laboratory 7600 Sandpoint Way NE, Seattle, WA 98115, USA 4- NOAA Atlantic Oceanographic and Meteorological Laboratory, Ocean Chemistry and Ecosystems Division 4301 Rickenbacker Cswy, Miami, FL 33149, USA University of Miami, Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science 4600 Rickenbacker Cswy, Miami, FL 33149, USA 5- Department of Marine Geosciences, University of Miami Rosenstiel School of Marine and Atmospheric Science4600 Rickenbacker Cswy, Miami, FL 33149, USA 6- Department of Geological Sciences, University of Miami 1320 S. Dixie Hwy, Coral Gables, FL 33124, USA Corresponding author: [email protected], +1-206-526-4287 Keywords: climate change; ocean acidification; warming; coral reefs; calcification; biomineralization; precipitation; dissolution; Florida Reef Tract; scleractinia Paper type: Original Research > Primary Research Article 1 Growth responses of Caribbean coral species ABSTRACT Anthropogenic climate change compromises reef growth due to increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. However, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification because data are lacking for many species. In order to address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27°C, 30.3°C) and CO2 partial pressures (pCO2) (400, 900, 1300 µatm). Mixed effects models of calcification for each species were then used to project community-level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO2. In the business-as-usual CO2 emissions scenario, reefs with high abundances of these species had projected end-of-century declines in scleractinian calcification of >50% relative to present-day rates. Siderastrea siderea, the other most-common species, was insensitive to both temperature and pCO2 within the levels tested here. Reefs dominated by this species had the most stable end- of-century growth. Under more optimistic scenarios of reduced CO2 emissions, calcification rates throughout the Florida Keys declined <20% by 2100. Under the most extreme emissions scenario, projected declines were highly variable among reefs, ranging 10 to 100%. Without considering bleaching, reef growth will likely decline on most reefs, especially where resistant species like S. siderea are not already dominant. This study demonstrates how species composition influences reef community responses to climate change and how reduced CO2 emissions can limit future declines in reef calcification. 2 Growth responses of Caribbean coral species INTRODUCTION Coral reefs are diverse ecosystems that vary in their coral species composition. This in turn shapes the underlying habitat and the species they support (Cheal et al., 2008, Hixon & Beets, 1993). As a result of the 2 Tt of anthropogenic CO2 emissions since the start of the Industrial Revolution (Le Quere et al., 2015), oceans are experiencing unprecedented rates of pH decline (“ocean acidification”) (Hönisch et al., 2012) and increased temperatures (Domingues et al., 2008). These changes deleteriously influence coral growth and cover through unfavorable chemistry and a disruption of the algal-coral symbiosis (“bleaching”) (Hoegh-Guldberg et al., 2007). Declining coral cover and calcification (Perry et al., 2013) reduce the architectural complexity of reefs (Alvarez-Filip et al., 2009) and cause cascading negative effects on habitat, diversity, and biomass (Paddack et al., 2009, Rogers et al., 2014, Wilson et al., 2006). Most studies conclude reef growth will slow significantly by the end of the century (Chan & Connolly, 2013, Hoeke et al., 2011, Kleypas et al., 1999, Kleypas & Yates, 2009, Langdon et al., 2000) or even cease by mid-century (Silverman et al., 2009). Assumed uniform coral responses to increased temperature and partial pressure of CO2 (pCO2) are often used in these modeling exercises (Buddemeier et al., 2008, Evenhuis et al., 2015, Silverman et al., 2009) because data on species-level responses are limited. In general, calcification has been measured as a Gaussian function of temperature (Jokiel & Coles, 1977, Marshall & Clode, 2004) at the organismal level, and a linear function of temperature across latitude (Lough & Barnes, 2000). Bleaching often sets the upper thermal limit to calcification by depriving corals of photosynthate, a key energy source. Bleaching thresholds are usually within 1-2ºC of summertime means (Coles et al., 1976, Jokiel & Coles, 1977). With respect to pCO2, calcification is often fit as a linear or n power law function k(Ωarag - 1) of aragonite saturation state (Ωarag), a carbonate chemistry 3 Growth responses of Caribbean coral species parameter inversely proportional to pCO2. However, compilations and meta-analyses have shown the slope of the calcification- Ωarag relationship varies across published literature (Chan & Connolly, 2013, Kleypas & Langdon, 2006, Langdon & Atkinson, 2005). These differences can be attributed to both species and the experimental methods though species-specific responses have been measured within the same study where methods and conditions were consistent (Comeau et al., 2013). Variation in Ωarag sensitivity among species and the ability of corals to regulate the chemistry within the calcifying space (McConnaughey, 2003) indicate species composition will determine how reefs respond to climate change. Predictions based on uniform constants therefore may not reflect future CaCO3 precipitation of individual reefs. Underscoring how reefs may vary in their responses to climate change, recent studies of reefs under elevated pCO2 have documented stable states ranging from reduced growth (Fabricius et al., 2011, Manzello, 2010) to tolerance (Shamberger et al., 2014, Shamberger et al., 2011) to phase shifts to macroalgae-dominated systems (Enochs et al., 2015). Furthermore, temperature often exerts a larger measurable influence on growth than Ωarag (Carricart-Ganivet et al., 2012, Helmle et al., 2011, Venti et al., 2014). This pattern is not surprising when the relative sensitivities of coral growth to temperature and Ωarag are compared to the annual variation of each parameter. In the Florida Keys, mean monthly temperature and Ωarag range from 23 to 30°C and 3.1 to 4.6 units, respectively (Fig. S1) (Kuffner et al., 2015, Sutton et al., 2014). Beyond this 7°C temperature range coral growth slows and eventually ends with mortality (Jaap, 1984, Vaughan, 1916, Vaughan & Wells, 1943).In contrast, the 1.5 unit Ωarag range would only affect -1 calcification by 23% (assuming a uniform 15% Ωarag sensitivity from Chan and Connolly (2013)). Future increases in temperature could increase net annual calcification over certain timescales depending on corals’ thermal optima (Jokiel & Coles, 1977). However, sustained 4 Growth responses of Caribbean coral species elevated temperatures can acutely stress corals and eventually induce bleaching and mortality. Conversely, decreased Ωarag will chronically depress calcification year-round. These different timescales and effect sizes highlight the need for studies testing coral responses to both increased temperature and pCO2. The first goal of this experiment was to assay calcification of twelve common Caribbean species under elevated temperature crossed with elevated pCO2 in the same experimental conditions (seasonality, duration, feeding, light, etc.). The control temperature of 27°C was chosen as representing the thermal optimum for these species in this region (Carricart-Ganivet et al., 2012, Kennedy et al., 2013) and is near the present-day mean annual temperature in the Florida Keys, where these species were collected. The elevated treatment temperature was set at 30.3°C, near the 30.5°C bleaching threshold for the Florida Keys based on NOAA’s climatological bleaching model (Manzello et al., 2007). The study species were Acropora cervicornis, Agaricia agaricites, Dichocoenia stokesii, Montastraea cavernosa, Orbicella faveolata, Porites astreoides, Porites divaricata, Pseudodiploria clivosa, Pseudodiploria strigosa, Siderastrea siderea, Siderastrea radians, and Solenastrea hyades. These species were chosen because of their current or historic abundance and/or because data are sparse on their growth responses to increased temperature and pCO2. The second goal was to test whether reef-
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