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Responses of Coral Reef Community Metabolism in Flumes to Ocean Acidification

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Responses of Coral Reef Community Metabolism in Flumes to Ocean Acidification Marine Biology (2018) 165:66 https://doi.org/10.1007/s00227-018-3324-0 ORIGINAL PAPER Responses of coral reef community metabolism in flumes to ocean acidification R. C. Carpenter1 · C. A. Lantz1,2 · E. Shaw1 · P. J. Edmunds1 Received: 4 June 2017 / Accepted: 8 March 2018 / Published online: 17 March 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract Much of the research on the effects of ocean acidification on tropical coral reefs has focused on the calcification rates of individual coral colonies, and less attention has been given to carbonate production and dissolution at the community scale. Using flumes (5.0 × 0.3 × 0.3 m) located outdoors in Moorea, French Polynesia, we assembled local back reef communities with ~ 25% coral cover, and tested their response to pCO2 levels of 344, 633, 870 and 1146 μatm. Incubations began in late G P Austral spring (November 2015), and net community calcification ( net) and net community primary production ( net) were measured prior to treatments, 24 h after treatment began, and biweekly or monthly thereafter until early Austral autumn G (March 2016). net was depressed under elevated pCO2 over 4 months, although the magnitude of the response varied over G Ω Ω time. The proportional decline in net as a function of saturation state of aragonite ( ar) depended on the initial ar, but was Ω Ω 24% for a decline in ar from 4.0 to 3.0, which is nearly twice as sensitive to variation in ar than the previously published G Ω values for the net calcification of ex situ coral colonies. However, community net was less sensitive to ar than coral reefs P P G that have been analyzed in situ. net was unaffected by pCO2, but net and net expressed on a hourly time base were positively G associated, thus revealing the tight coupling between these metabolic processes. The high sensitivity of net to pCO2 for the back reef of Moorea, versus lower sensitivity of individual coral colony calcification to pCO2, underscores the challenges of scaling-up experimental results on the effects of pCO2 from coral reef organisms to coral reef communities. Introduction partial pressure of CO 2 (pCO2), thereby decreasing seawater Ω pH and the saturation state ( ) of calcium carbonate [CaCO3 Ω Ω Coral reefs are one of the most vulnerable ecosystems to as aragonite ( ar) and calcite ( ca)] without affecting total A ocean acidification (Kleypas and Yates 2009), which is the alkalinity ( T) (Doney et al. 2009). It is widely recognized product of increasing anthropogenic carbon dioxide (CO 2) that these effects will decrease the rates at which many emissions, and the dissolution of CO2 in seawater. The dis- coral reef calcifiers deposit CaCO 3 (Kroeker et al. 2013; solution of CO2 into the surface ocean elevates the aqueous Comeau et al. 2014a), and increase the CaCO3 dissolution of reef communities (Andersson and Gledhill 2013; Eyre et al. 2014; Comeau et al. 2016). Combined, these trends are G Responsible Editor: R. Hill. expected to cause community net calcification ( net, gross calcification minus dissolution) to decline on coral reefs, Reviewed by T. DeCarlo and undisclosed experts. and potentially degrade structural habitat complexity that Electronic supplementary material The online version of this is formed through biogenic calcification (Hoegh-Guldberg article (https ://doi.org/10.1007/s0022 7-018-3324-0) contains et al. 2007; Comeau et al. 2016). supplementary material, which is available to authorized users. G In situ measurements of coral reef community net have shown that it is affected by natural diel variations in seawater * R. C. Carpenter [email protected] carbonate chemistry (Shaw et al. 2012). For example, G r2 net was associated significantly ( = 0.33) with diurnal 1 Ω Department of Biology, California State University, 18111 variation in ar (with a median diurnal variation of 3.25) Nordhoff Street, Northridge, CA 91330-8303, USA at Lady Elliot Island, Australia (Shaw et al. 2012). Based 2 Ω School of Environmental Science and Engineering, Southern on field measurements of the relationships between ar and Cross University, Military Road, East Lismore, NSW 2480, G , Silverman et al. (2009) predicted that coral reefs would Australia net Vol.:(0123456789)1 3 66 Page 2 of 13 Marine Biology (2018) 165:66 transition from net calcification to net dissolution at 560 ppm et al. 2011; Frieder et al. 2016), and it can also create a pH atmospheric pCO2, which potentially could occur within environment favoring calcium carbonate deposition (Alle- 50 years (IPCC, 2014). However, for scleractinian corals that mand et al. 2011). For coral reefs, evidence that ocean acidi- P are the ecosystem engineers of coral reefs (Jones et al. 1994; fication affects net at any level of biological organization is Wild et al. 2011) and a major contributor to their CaCO 3 equivocal (Anthony et al. 2008a; Crawley et al. 2010; Dove production (Perry et al. 2013), there is interspecific variation et al. 2013; Comeau et al. 2016); however, the relationship P G in the sensitivity of calcification to increases in pCO 2 (Chan between community net and net can be altered by ocean and Connolly 2013; Comeau et al. 2014a). The calcification acidification (DeCarlo et al. 2017), reflecting a disruption of rates of many species are affected strongly and negatively by the coupling between organic and inorganic carbon fixation. high pCO2 (Chan and Connolly 2013; Comeau et al. 2014a), In situ analyses of coral reef community metabolism (i.e., G P but in some species, they are affected less severely (Comeau net and net) typically use short experiments in which meas- et al. 2014a). The sensitivity of calcification to pCO2 can be urements employing the alkalinity anomaly techniques (Kin- both species and life history stage specific and related to the sey 1978; Smith and Kinsey 1978) are completed over min- extent to which organisms are able to biologically control utes-to-days (Gattuso et al. 1996; Shaw et al. 2015; DeCarlo the calcification process (Comeau et al. 2014a). Generally, et al. 2017). This resolution reflects the need to constrain net calcification of individual coral species appears to be some experimental work to periods with reduced seawater less sensitive to elevated pCO 2 than it is for the coral reef flow (e.g., slack water), but it also is important to detect G communities they build (Pandolfi et al. 2011; Comeau et al. rapid changes in community net, such as how it occurs in 2015; 2016). response to diel variation in carbonate chemistry (Ohde It is unknown, however, whether the greater sensitivity and van Woesik 1999; Shaw et al. 2012). Other approaches G of coral reef community net to ocean acidification, relative (e.g., Lagrangian transects) quantify metabolic rates over to coral colonies, reflects methodological artifacts, or is the one to several days (e.g., Kinsey 1985; Gattuso et al. 1996). result of emergent properties of the communities, for exam- To date, however, there is limited evidence of the extent to ple, the propensity of some of their inorganic components which short-term experiments and measurements are indica- for dissolution (Andersson and Gledhill 2013; Eyre et al. tive of responses occurring over months-to-years (Kroeker 2014). Unlike the laboratory experiments that typically are et al. 2013). The present study is part of a larger project employed to study the response of corals to elevated pCO2, to measure the metabolic response of coral reef communi- when in situ approaches are used to evaluate the relationship ties to elevated pCO2 over ecologically relevant time scales, G between community net for coral reefs and pCO2, it is dif- and here we present the results from the first 4 months of ficult methodologically to control seawater pCO 2 or pH pre- this experiment. Working with a benthic community from cisely to simulate future conditions (although see Albright the back reef of Moorea, French Polynesia, we present the et al. 2016). The other conditions that are likely to covary results of an experiment in which we measured community G P with pCO2 include light availability, seawater temperature, net and net under four pCO 2 regimes from late Austral G nutrient concentrations, and flow regimes, all of which could spring to early Austral autumn. Using community net and G P affect the response of community net to seawater carbonate net as dependent variables, we tested the hypothesis that chemistry (Comeau et al. 2014b). The quality and quantity the effects of pCO2 are consistent over times-scales ranging of light, for example, affects community net photosynthesis from 1 day to 4 months. As a means to test our hypothesis, P G ( net) on coral reefs, which is a driver of community net we also explored the effects of pCO2 on diel variation in P G P (Kinsey 1985; Falter et al. 2008), but community net also community net and net as well as the degree to which these affects seawater carbonate chemistry through the uptake of variables were associated. dissolved inorganic carbon [(DIC), Anthony et al. 2008b; Shaw et al. 2012]. Together, these effects cause community Methods G net to be associated with seawater carbonate chemistry, P light availability, and community net (Falter et al. 2012). Rates of primary production on coral reefs primarily Coral reef communities were assembled in four, outdoor are driven by light availability, but they can be modified by flumes in Moorea, French Polynesia. Logistical constraints additional factors such as temperature, nutrient availability, of constructing, instrumenting, and maintaining additional and water flow (Dennison and Barnes 1988; Atkinson et al. flumes precluded an experimental design with replicate P G 1999; Langdon and Atkinson 2005). net and net typically flumes for each pCO 2 treatment.
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