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Accepted Manuscript1.0 -RXUQDORI([SHULPHQWDO0DULQH%LRORJ\DQG(FRORJ\ ² Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Effect of elevated pCO2 on competition between the scleractinian corals Galaxea fascicularis and Acropora hyacinthus ⁎ Nicolas R. Evensena,b, , Peter J. Edmundsa a Department of Biology, California State University, 18111 Nordhoff Street, Northridge, CA 91330-8303, USA b Marine Spatial Ecology Lab, Australian Research Council Centre of Excellence for Coral Reef Studies and School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia ARTICLE INFO ABSTRACT Editor: M. Donahue Ocean acidification is expected to affect coral reefs in multiple ways, in part, by depressing the calcification of fi Keywords: scleractinian corals. To evaluate how coral communities will respond to ocean acidi cation, research into the Ocean acidification effects on ecological processes determining community structure is now needed. The present study focused on Species interactions corals utilizing soft tissues (i.e., mesenterial filaments) as agonistic mechanism, and evaluated their ability to Mesenterial filaments compete for space under ocean acidification. Using aquarium-reared specimens in Monaco, single polyps of Competition for space Galaxea fascicularis were paired with branch tips of Acropora hyacinthus to stimulate competitive interactions, which were evaluated through the production and use of mesenterial filaments in causing tissue damage under ambient (~600 μatm) and elevated pCO2 (~1200 μatm). At 1200 μatm pCO2, and when paired with A. hya- cinthus, the extrusion of mesenterial filaments from G. fascicularis occurred 2 days earlier than under ambient pCO2, although ultimately the mesenterial filaments caused the same amount of tissue necrosis on A. hyacinthus under both pCO2 regimes after 7 days. This outcome supports the hypothesis that some kinds of competitive mechanisms utilized by scleractinian corals (i.e., mesenterial filaments) will be unaffected by short exposure to pCO2 as high as 1200 μatm. 1. Introduction topographically complex surfaces (Fabricius et al., 2011), and to com- pete for space with other organisms (Diaz-Pulido et al., 2011; Connell Global climate change and ocean acidification (OA) are affecting a et al., 2013). variety of abiotic conditions in the marine environment (Kleypas et al., There is strong variation among scleractinian species in the extent 2006; Hoegh-Guldberg et al., 2007), making it important to understand to which their calcification is reduced by low pH (Chan and Connolly, the physiological response of individuals to these predicted changes in 2013), with fast-growing corals more sensitive to OA than slow-growing environmental conditions. However, it is also important to understand corals (Comeau et al., 2014; Shaw et al., 2016). This is an important how these changes will affect ecological processes mediating interac- observation, as speed of growth is associated with competitive ability in tions among organisms in order to evaluate the consequences of OA on scleractinians, with fast growing corals able to exploit overgrowth as a entire communities (Gaylord et al., 2015). For example, on tropical competitive mechanism favouring spatial dominance (Connell et al., coral reefs, short-term experiments (8 weeks) suggest that the outcome 2004). In contrast, corals that grow slowly typically employ a range of of competitive interactions between coral and macroalgae may shift to alternative mechanisms to compete for space, including sweeper favour dominance by macroalgae due to OA (1140 μatm pCO2; Diaz- polyps, sweeper tentacles, or mesenterial filaments (Lang and Pulido et al., 2011). Further, as tropical corals will be exposed in Chornesky, 1990). Mesenterial filaments are primarily used for diges- coming decades to declining seawater pH and reduced seawater sa- tion (Wijgerde et al., 2011), as well as to capture particles outside of the turation state with respect to aragonite (Ωarag) attributed to OA, their polyp (Smith et al., 2016), but they can also be used for spatial com- capacity to rapidly calcify is likely to be challenged (Orr et al., 2005). petition (Lang and Chornesky, 1990; Nugues et al., 2004). In this role, Ultimately, impaired rates of calcification will affect coral reef com- mesenterial filaments are typically deployed to attack the tissue of munities (Anthony et al., 2011; Edmunds et al., 2016) through a variety competitors growing a few centimetres away (Goreau et al., 1971; of mechanisms including a reduction in the ability of corals to form Sheppard, 1979), thereby maintaining free space for future growth, and ⁎ Corresponding author at: Marine Spatial Ecology Lab, Australian Research Council Centre of Excellence for Coral Reef Studies and School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia. E-mail address: [email protected] (N.R. Evensen). https://doi.org/10.1016/j.jembe.2017.12.002 Received 19 February 2017; Received in revised form 5 November 2017; Accepted 1 December 2017 (OVHYLHU%9$OOULJKWVUHVHUYHG N.R. Evensen, P.J. Edmunds -RXUQDORI([SHULPHQWDO0DULQH%LRORJ\DQG(FRORJ\ ² selecting nubbins of each species, and pairing them on custom-made PVC supports that held them 90° to one another (Fig. 1). Corals were fixed in this arrangement using epoxy (Aquastik), and were secured with a ~1 mm gap between them to stimulate a competitive encounter (sensu Chornesky, 1983). Two Galaxea-Acropora pairings were created in each of four tanks, with two incubated at ambient pCO2 (i.e., controls) and two at elevated pCO2. The tanks were maintained at 24.95 ± 0.03 °C (mean ± SE, n = 48) and illuminated by metal halide lamps (Philips, HPIT 400 W, Distrilamp, Bossee, France) on a 12:12 light:dark photoperiod with − − intensities of ~250 ± 20 μmol photons m 2 s 1, measured beneath the seawater using a 4π quantum sensor (Li-Cor, Li-193SA). Controls tanks were filled with ambient seawater, and experimental tanks were manipulated to an elevated pCO2 of ~1200 μatm, representative of Fig. 1. Diagram showing arrangement of Acropora hyacinthus (left) next to Galaxea fas- predicted CO concentrations in the atmosphere by the end of the cicularis (right). Corals were fixed to microscope slides by their bases, and the slides were 2 used to position the corals normal (90°) to one another on a PVC support to maintain a century under the representative concentration pathway 8.5 (Moss small separation between them. et al., 2010). Carbonate chemistry in the seawater was modified in the elevated pCO2 treatment by bubbling pure CO2 into the seawater with a pH-controlling system (Apex Aquacontroller, Neptune Systems, USA). reducing the likelihood that digestively aggressive corals will be over- grown by fast growing competitors (Chadwick, 1987; Bruno and 2.2. Carbonate chemistry Witman, 1996). Thus, agonistic mechanisms, such as mesenterial fila- ments, play important roles for many scleractinians to maintain space Seawater pHT was monitored daily using a hand-held pH Meter on the reef. While the effects of elevated pCO2 on the growth of scler- (Odeon, Ponsel) that was calibrated on the total scale using 2-amino-2- actinians has been studied in detail (Chan and Connolly, 2013; Comeau hydroxymethyl-1,3-propanediol (TRIS) buffers at a salinity of 38.0 et al., 2013; Okazaki et al., 2016), the effects of OA on the formation (Dickson et al., 2007). pH also was measured every other day spec- and deployment of agonistic mechanisms has not been explored. T trophotometrically in every tank using the indicator dye m-cresol The objective of this study was to evaluate the effects of OA on (Standard operating procedure 6b, Dickson et al., 2007). Total alkali- mesenterial filament extrusion during competitive interactions among nity (A ) was measured daily using open-cell potentiometric titrations corals, and to assess the extent of tissue damage created on competitors T completed with an automatic titrator (Metrohm Titrando 888 Dosimat). by mesenterial filaments at elevated pCO2. Using a coral culture facility Measurements of A were conducted on duplicate 4 mL samples at room in Monaco, single polyps of Galaxea fascicularis were paired with T temperature (~23 °C), and A was calculated using a Gran function branch tips of Acropora hyacinthus (Fig. 1) to stimulate competitive T applied to pH values ranging from 3.0 to 3.5 (after Dickson et al., interactions under ambient or elevated pCO2 and test the hypothesis 2007). Measurement accuracy and precision were ensured using certi- that pCO2 has no effect on the use of mesenterial filaments in coral- fied reference materials from the A. G. Dickson laboratory (Dickson coral competition. While both species are strong competitors for space et al., 2007). Parameters of the carbonate system in seawater were on shallow reefs in the Red Sea (Abelson and Loya, 1999), Galaxea spp. calculated from salinity, temperature, A and pH using the R package is more aggressive than Acropora spp. (Sheppard, 1979; Dai, 1990; T T Seacarb (Lavigne and Gattuso, 2013). Horwitz et al., 2017). 2.3. Observations of competitive encounters 2. Methods Interactions between paired corals were evaluated at the start of the 2.1. Experimental design experiment, after 6 h, and then after 1, 2, 4, 6, and 7 d incubations. Each time-point was used as a replicate for the ‘time’ factor in the This study was completed in April 2014 in Monaco, using corals PERMANOVA (described below). Evaluations
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