Impacts of Food Availability and Pco2 on Planulation, Juvenile Survival, and Calcification of the Azooxanthellate Scleractinian Coral Balanophyllia Elegans
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UC Irvine UC Irvine Previously Published Works Title Impacts of food availability and pCO2 on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral Balanophyllia elegans Permalink https://escholarship.org/uc/item/4zp5n82m Journal Biogeosciences, 10(11) ISSN 1726-4170 Authors Crook, ED Cooper, H Potts, DC et al. Publication Date 2013-12-02 DOI 10.5194/bg-10-7599-2013 Supplemental Material https://escholarship.org/uc/item/4zp5n82m#supplemental License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Biogeosciences, 10, 7599–7608, 2013 Open Access www.biogeosciences.net/10/7599/2013/ doi:10.5194/bg-10-7599-2013 Biogeosciences © Author(s) 2013. CC Attribution 3.0 License. Impacts of food availability and pCO2 on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral Balanophyllia elegans E. D. Crook1, H. Cooper2, D. C. Potts2, T. Lambert1, and A. Paytan1 1University of California, Santa Cruz, Department of Earth and Planetary Sciences, 1156 High Street, Santa Cruz, CA 95064, USA 2University of California, Santa Cruz, Department of Ecology and Evolutionary Biology, 1156 High Street, Santa Cruz, CA 95064, USA Correspondence to: E. D. Crook ([email protected]) Received: 30 March 2013 – Published in Biogeosciences Discuss.: 7 May 2013 Revised: 7 October 2013 – Accepted: 10 October 2013 – Published: 22 November 2013 Abstract. Ocean acidification, the assimilation of atmo- but not wider at 1220 µatm. We conclude that food abun- spheric CO2 by the oceans that decreases the pH and dance is critical for azooxanthellate coral calcification, and CaCO3 saturation state () of seawater, is projected to that B. elegans may be partially protected from adverse con- have severe adverse consequences for calcifying organisms. sequences of ocean acidification in habitats with abundant While strong evidence suggests calcification by tropical reef- heterotrophic food. building corals containing algal symbionts (zooxanthellae) will decline over the next century, likely responses of azoox- anthellate corals to ocean acidification are less well under- stood. Because azooxanthellate corals do not obtain photo- 1 Introduction synthetic energy from symbionts, they provide a system for studying the direct effects of acidification on energy avail- As aqueous CO2 concentrations continue to rise over the able for calcification. The solitary azooxanthellate orange next century, pH of oceanic surface waters will decline in the cup coral Balanophyllia elegans often lives in low-pH, up- process known as ocean acidification (Caldeira and Wicket, welled waters along the California coast. In an 8-month fac- 2003, 2005; Sabine et al., 2004). Growing evidence sug- torial experiment, we measured the effects of three pCO2 gests that calcifying organisms, including reef-building scle- treatments (410, 770, and 1220 µatm) and two feeding fre- ractinian corals, will be heavily impacted by a decrease in quencies (3-day and 21-day intervals) on “planulation” (lar- pH from 8.1 to 7.8 (Orr et al., 2005; Hoegh-Guldberg et al., val release) by adult B. elegans, and on the survival, skeletal 2007; Fabry et al., 2008; Doney et al., 2009). In many labo- growth, and calcification of newly settled juveniles. Planula- ratory and field investigations, calcification rates of tropical tion rates were affected by food level but not pCO2. Juvenile corals declined as pH and aragonite saturation state (arag, mortality was highest under high pCO2 (1220 µatm) and low a measure of ease of CaCO3 formation) decreased (Fine and food (21-day intervals). Feeding rate had a greater impact Tchernov, 2007; Anthony et al., 2008; Jokiel et al., 2008; on calcification of B. elegans than pCO2. While net calci- Krief et al., 2010). Almost all tropical corals have algal sym- fication was positive even at 1220 µatm (∼ 3 times current bionts (zooxanthellae) whose photosynthesis contributes to atmospheric pCO2), overall calcification declined by ∼ 25– the host’s nutrition and increases calcification rates. Most 45 %, and skeletal density declined by ∼ 35–45 % as pCO2 deep and cold-water corals lack zooxanthellae, but their po- increased from 410 to 1220 µatm. Aragonite crystal morphol- tential responses to ocean acidification are largely unknown; ogy changed at high pCO2, becoming significantly shorter as the saturation state of seawater decreases, their calcifica- tion rates are also likely to decline and their geographical Published by Copernicus Publications on behalf of the European Geosciences Union. 7600 E. D. Crook et al.: Impacts of food availability and pCO2 on planulation, juvenile survival, and calcification distributions may change (Turley et al., 2007; Andersson et ration states of the calcifying fluids, and perhaps enable them al., 2008; Fabry et al., 2009; Maier et al., 2009). Experi- to maintain calcification despite acidification. Some research ments indicate that cold-water species vary in sensitivity to indicates that zooxanthellate coral calcification is energeti- CO2 manipulation, and some deep-water species can main- cally costly and that a coral’s energy budget is not flexible tain positive net calcification at or below the carbonate satu- enough to raise the pH of the calcifying fluid under acidic ration horizon, the depth below which < 1 and CaCO3 can conditions (i.e., the energy budget is fixed) (Cohen and Hol- dissolve readily (Form and Riebesell, 2012; McCulloch et comb, 2009), but some species can maintain up to 100 % al., 2012; Maier et al., 2011). Because azooxanthellate corals of their calcification rates in near-undersaturated conditions lack symbionts and rely solely on heterotrophy for energy, when provided with excess nutrients (Langdon and Atkin- they provide a simplified system for exploring the roles of son, 2005; Holcomb et al., 2010, Ries et al., 2009; Cohen et nutrition (and energy) in coral calcification. al., 2009). Nutrients may stimulate increased photosynthesis Ocean acidification is predicted to have especially severe by zooxanthellae, giving the coral more energy for calcifi- impacts in upwelling regions where low-saturation waters cation. Similarly, increased heterotrophic feeding by certain occur naturally (Feely et al., 2008; Fabry et al., 2009; Hauri zooxanthellate corals can reduce acidification impacts on cal- et al., 2009). Strong seasonal upwelling along the western cification (Drenkard et al., 2013, Edmunds, 2011). All corals North American coast during summer months brings CO2- in these studies contained energy-producing zooxanthellae, rich, low-pH water from intermediate depths to the surface, whereas azooxanthellate corals cannot obtain extra photo- and coastal organisms may be exposed to low-saturation and synthetic energy from symbionts. Therefore azooxanthellate even undersaturated waters for several months of the year corals provide a system in which it is possible to study the (Feely et al., 2008; Hauri et al., 2009). With anticipated in- direct effects of ocean acidification and energy availability creases in surface ocean pCO2 and shoaling of the carbon- on calcification. ate saturation horizon, calcifying organisms living in these Balanophyllia elegans is a solitary, azooxanthellate scle- coastal waters are likely to experience seasonal increases in ractinian coral common in shallow coastal waters around the magnitude, duration, and extent of low-pH waters (Feely Monterey Bay, California, where it is exposed seasonally to et al., 2008; Hauri et al., 2009). Understanding the impacts of low-pH, high-pCO2 upwelling waters. We assessed the ef- ocean acidification on calcification and on the interplay be- fects of pCO2 and food availability on planulation rates of tween calcification and nutritional status is critically impor- adult B. elegans, and then explored the effects of the same tant in upwelling regions where many organisms may already treatments on survival, growth, and calcification of juvenile be living near their lower thresholds for pH tolerance (Bar- B. elegans during an 8-month incubation experiment. The du- ton et al., 2012) and therefore may be particularly vulnerable ration was based on recommendations of Doney et al. (2009) to ocean acidification. Several recent studies have described and Widdicombe et al. (2010) for long-term manipulation likely negative consequences of future ocean acidification experiments. Recent evidence suggests that long-term ex- events for several key species in the California coastal up- posure more accurately predicts responses to acidification welling zone (Gaylord et al., 2011; Barton et al., 2012; Het- than short-term experiments (Form and Riebesell, 2012). We tinger et al., 2012; Timmins-Schiffman et al., 2012), which address how azooxanthellate corals may respond to lower often experiences seawater pH as low as 7.8 during the sum- ocean pH, and the roles of nutrition on their calcification and mer. survival in low-saturation, upwelling regimes. Responses of calcifying corals to ocean acidification de- pend on species-specific energy allocations for calcification. Corals expend energy to remove protons from their calci- 2 Materials and methods fying compartments, the extracellular medium between the coral’s basal cell membrane and the skeleton below (Al Ho- 2.1 Organisms rani et al., 2003; Allemand et al., 2004; Cohen and Mc- Connaughey, 2003). Removing protons facilitates calcifica- The orange cup coral Balanophyllia elegans Verrill, 1864, is tion by increasing pH and CaCO3