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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 were made at 08:00 h collected from the Red Sea and maintained for years in aquaria at the before the lights were switched on, as competitive interactions between Centre Scientifique de Monaco (CSM) (Houlbrèque et al., 2004; corals are more prevalent at night (Lang, 1973; Nugues et al., 2004). Reynaud et al., 2007). Nubbins were prepared from one colony of each Paired corals were removed from the tanks and placed in individual species (i.e., a single genotype) and arranged in competitive pairings dishes without exposing the coral tissues to air. Each observation con- juxtaposing single polyps of Galaxea fascicularis with single branch tips sisted of a 5-minute video of the contact zone (an area of ~2 × 2 cm) of Acropora hyacinthus (both ~15-mm long). Replicate configurations between the corals, and it was recorded under red light using a digital were incubated for 7 d under ambient and elevated pCO2 (targeted at USB Microscope (×10 magnification, 2.0 megapixel resolution, VMS- 1200 μatm), with the response evaluated by the competitive interac- 004 Discovery Deluxe, Veho, UK) connected to a computer. Using video tions between the corals, as quantified by mesenterial filament extru- clips as a record of the interactions, the number of extruded mesenterial − − sion (mesenterial filaments polyp 1 time 1) and the extent of tissue filaments for each coral was counted. Still images (taken with a Canon damage (mm2) to the subordinate coral (Fig. 2). S95; 10-megapixel resolution) of the interactions that included a scale Single polyps of Galaxea fascicularis were removed from the parent bar were used to quantify tissue necrosis using ImageJ software (v1.46; colony with pliers, and attached by their bases to microscope slides. Rasband, 1997) at the end of the incubation. Branch tips of Acropora hyacinthus were cut from parent colonies in a similar way, and fixed vertically to microscope slides by their bases. In 2.4. Statistical analysis both cases, coral pieces were glued to microscope slides using cya- noacrylate glue (Loctite™), and left to recover for 2 d in flow-through Physical and chemical conditions in the tanks, as well as area of aquaria; 8 slides were prepared for each species. Following recovery, tissue necrosis for A. hyacinthus colonies, were compared among tanks slides were randomly allocated to ambient or elevated pCO2 treatments with two-way ANOVAs (performed using R software; R Foundation for in four 20-L tanks, and allowed to acclimate for one week. For each Statistical Computing), with pCO2 as a fixed effect and tank a random treatment, four interspecific pairings were created by randomly factor nested in each pCO2 treatment; the tank effect was dropped from

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Fig. 2. Photographs of competitive pairings between Acropora hyacinthus (A) and Galaxea fascicularis (G). Top row shows a pairing incubated under ambient pCO2 on day one of the incubation (left), and after four days (right). Bottom row shows a pairing incubated under high pCO2 (~1200 μatm) on day one of the incubation (left), and after four days (right). Mesenterial filaments extruded by G. fascicularis (G) are indicated by the red arrows. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) the analyses when not significant at p ≥ 0.25 (Quinn and Keough, During the experiment, only one A. hyacinthus was observed pro- 2002). ducing mesenterial filaments, and therefore the analysis focused on A permutational ANOVA (PERMANOVA) was used to analyze the mesenterial filaments extruded by G. fascicularis, each of which released effects of pCO2 on the number of mesenterial filament extruded by the multiple mesenterial filaments throughout the experiment. For G. fas- interacting corals. PERMANOVA was conducted using PRIMER-E v6 cicularis, the extrusion of mesenterial filament differed over time software (Clarke and Gorley, 2006) with the PERMANOVA+ extension (Pseudo-F5,10 = 4.14, p = 0.032), and the effect of time differed be- (Anderson et al., 2008), using pCO2 and time as fixed factors, and tank tween pCO2 treatments (i.e., the time × pCO2 interaction was sig- as a random factor nested in pCO2. PERMANOVA was performed on a nificant: Pseudo-F5,10 = 3.64, p = 0.043). This interactive effect was similarity matrix of Euclidean distances among replicates, with tests noticeable on the 4th day of the incubation, when G. fascicularis at −1 based on 9999 unrestricted permutations of the raw data (Anderson elevated pCO2 extruded 5–15 mesenterial filament polyp (with each et al., 2008). filament ~5-mm long), while none was observed for polyps at ambient

treatment pCO2 until day 6 (Fig. 3). From day 6 onwards, G. fascicularis − under ambient pCO also extruded 5–15 mesenterial filament polyp 1. 3. Results 2 Thereafter, mesenterial filament extrusion decreased in both treatments as parts of the adjacent A. hyacinthus colonies were killed by me- Conditions within the tanks were precisely regulated (Table 1), with senterial filament contact. Overall, there was no statistically significant analysis of seawater chemistry revealing that pH differed between effect of pCO on mesenterial filament extrusion (Pseudo-F = 7.20, treatments (F = 503, p < 0.001), but not among tanks within each 2 1,2 1,2 p = 0.346), despite more mesenterial filaments extruded at elevated pCO2 treatment (F2,44 = 0.011, p = 0.915). Similarly, pCO2 and ΩArag −1 pCO2 (2.83 ± 0.58 mesenterial filament polyp ) than ambient pCO2 differed between treatments (F ≥ 335, p < 0.001), but not within − 1,2 (1.83 ± 0.23 mesenterial filament polyp 1; n = 4). each pCO treatment (F ≤ 0.025, p ≥ 0.876). Temperature and 2 2,44 For the analysis of tissue necrosis at the end of the incubation (day total alkalinity (A ) did not differ between tanks (F ≤ 0.629, T 2,44 7), tanks were pooled, as there was no difference between tanks within p ≥ 0.432). Overall, the treatments contrasted a pCO of 2 pCO treatments (F = 0.657, p = 0.566). However, dropping tanks 593 ± 7 μatm (ambient for laboratory seawater) with 2 2,4 from the model did not affect the outcome of the analysis, and therefore 1193 ± 40 μatm (elevated pCO2 treatment) (mean ± SE, n = 12).

Table 1

Physical conditions and carbonate chemistry in tanks during incubations. Values shown are mean ± SE (n = 12). ACO2 = Ambient pCO2, HCO2 = High pCO2 (target was 1200 μatm).

− 1 Treatment Tank T (°C) pHT pCO2 (μatm) AT (μmol kg ) ΩArag

HCO2 1 25.0 ± 0.1 7.67 ± 0.01 1188 ± 42 2488 ± 4 1.81 ± 0.06 2 25.0 ± 0.1 7.66 ± 0.02 1199 ± 48 2485 ± 3 1.80 ± 0.06

ACO2 3 24.9 ± 0.1 7.93 ± 0.01 594 ± 9 2488 ± 3 2.99 ± 0.03 4 25.0 ± 0.1 7.93 ± 0.01 593 ± 7 2492 ± 5 3.01 ± 0.04

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Fig. 3. Rate of mesenterial filament extrusion (mean ± SE, 30 Day 7 15 n = 4) as a function of time for Galaxea fascicularis polyps in- 2 pCO treatment cubated under ambient (593 μatm) and high pCO (1193 μatm). 2 2 2 Ambient Inset: Mean extent of tissue necrosis (mm ) ( ± SE, n =4)on 20 Elevated Acropora hyacinthus branch tips at the end of 7 d incubations

under each pCO2 treatment.

10 10 Area of tissue necrosis (mm ) necrosis of tissue (mm Area

0 Ambient Elevated Treatment

5 Mesenterial filaments polyp filaments Mesenterial

0

6 hours Day 1 Day 2 Day 4 Day 6 Day 7 Time the full model was run. Area of tissue necrosis did not differ between intermedia and the macroalga Lobophora papenfussii at elevated versus pCO2 treatments (F1,2 = 0.488, p = 0.557), with mean tissue necrosis ambient pCO2 (1140 μatm and 400 μatm, respectively) (Diaz-Pulido 2 of 27.6 ± 2.4 mm ( ± SE) on A. hyacinthus at elevated pCO2, and et al., 2011). In the study conducted by Diaz-Pulido et al. (2011), A. 2 24.1 ± 5.3 mm ( ± SE) on A. hyacinthus colonies at ambient pCO2 intermedia experienced a two-to-threefold reduction in survivorship (both n = 4). when competing with L. papenfussii under elevated pCO2 compared to ambient conditions. To our knowledge, only one study has investigated the effects of elevated pCO on the growth of competing corals, using 4. Discussion 2 species that use mechanisms other than rapid growth for this purpose (Horwitz et al., 2017). Overall, however, there still is little known about This study investigated the effects of elevated pCO on extrusion 2 the effects of OA on competitive mechanisms employed by corals. and efficacy of mesenterial filaments during competitive interactions For the coral Galaxea fascicularis, which can be common on Indo- between Galaxea fascicularis and Acropora hyacinthus. Incubating G. Pacific reefs, particularly in inshore habitats (McClanahan et al., 1999; fascicularis polyps adjacent to branch tips of A. hyacinthus under ele- Perry et al., 2009), evaluating its likely performance under OA condi- vated pCO resulted in mesenterial filaments extrusion earlier than 2 tions has become complex. This complexity arises from incongruent under ambient conditions, with the peak use of mesenterial filaments analyses of growth and competitive ability under OA, which report occurring 2 days before that observed under ambient pCO . Despite 2 reduced growth rates of G. fascicularis colonies under elevated pCO earlier extrusion, the extent of tissue necrosis caused on A. hyacinthus 2 (Marubini et al., 2003; Horwitz et al., 2017), but unimpaired capacity by mesenterial filaments was the same between pCO treatments at the 2 to compete and deploy agonistic competitive mechanisms (the present end of the 7 day incubation. While there is evidence that tropical study; Horwitz et al., 2017). In Eilat, for example, Horwitz et al. (2017), scleractinians grow and compete for space less effectively under OA reported a 55% reduction in linear growth of G. fascicularis at compared to ambient pCO (Diaz-Pulido et al., 2011), and that coral 2 ~1795 μatm pCO , which was the strongest reduction in growth for the reef communities can shift from coral- towards macroalgal- dominance 2 six corals that were studied (including Acropora variabilis, Pocillopora at elevated pCO (Dove et al., 2013), to date, the effects of pCO on the 2 2 damicornis, Stylophora pistillata, Cyphastrea chalcidicum, and Porites production and use of agonistic competitive mechanisms has not been lutea). In the same study, however, G. fascicularis had the highest ca- investigated for scleractinians. Our study demonstrates that elevated pacity of the corals studied to maintain growth in the presence of coral pCO does not negatively impact the ability of G. fascicularis to employ 2 competitors (i.e., the 5 other aforementioned study species) over 1-year mesenterial filaments as a means of spatial competition, at least in short (Horwitz et al., 2017). The results of Horwitz et al. (2017) indicate that incubations completed with cultivated corals under controlled labora- despite a strong reduction in growth under OA, elevated pCO does not tory conditions. 2 impair the capacity for coral-coral competition by G. fascicularis. Al- Research into the effects of OA on marine communities has started though the present study was conducted over 7 d, with limited re- to highlight the importance of the interplay between the effects on plication, the results for G. fascicularis are consistent with those ob- organism physiology and the effects on species interactions in driving tained over a much longer period for the same species (i.e., in Horwitz changes in community structure (Kroeker et al., 2013; Gaylord et al., et al., 2017), because both studies indicate a null effect of OA on coral- 2015). Overall, calcifying organisms, including scleractinians, tend to coral competition. Unlike Horwitz et al. (2017), however, the present calcify more slowly at elevated versus current ambient pCO (Kroeker 2 study focused on one proximal mechanism of competition, and showed et al., 2010; Chan and Connolly, 2013; Comeau et al., 2014). Con- that its effects (tissue necrosis on the subordinate coral) were not in- trastingly, some macroalgae can exploit elevated seawater pCO to 2 fluenced by OA, thus offering one explanation for a similar outcome enhance growth (Cornwall et al., 2012; Gaylord et al., 2015), and thus over a longer period (i.e., in Horwitz et al., 2017). may gain a competitive advantage over calcifiers in temperate and While corals exhibit a variety of competitive mechanisms, including tropical benthic communities exposed to elevated pCO (Connell et al., 2 overgrowth and shading (McCook et al., 2001), agonistic mechanisms, 2013; Kroeker et al., 2013). Evidence supporting this prediction comes such as mesenterial filaments, are employed by many species against from experimental investigations of interactions between Acropora

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both corals and macroalgae (Lang and Chornesky, 1990; McCook et al., coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping 2001; Nugues et al., 2004). Thus, the ability of corals to maintain the point. Limnol. Oceanogr. 58, 388–398. Comeau, S., Edmunds, P.J., Spindel, N.B., Carpenter, R.C., 2014. Fast coral reef calcifiers use of such agonistic mechanisms under elevated pCO2 may be im- are more sensitive to ocean acidification in short-term laboratory incubations. portant for other coral species in light of the increased presence of Limnol. Oceanogr. 59, 1081–1091. macroalgae on coral reefs (Burkepile and Hay, 2006), and the potential Connell, J.H., Hughes, T.P., Wallace, C.C., Tanner, J.E., Harms, K.E., Kerr, A.M., 2004. A fi long-term study of competition and diversity of corals. Ecol. Monogr. 74, 179–210. for macroalgae to physiologically bene t from elevated pCO2 (Connell Connell, S.D., Kroeker, K.J., Fabricius, K.E., Kline, D.I., Russell, B.D., 2013. The other et al., 2013). Additionally, while the energetic costs of deploying soft- ocean acidification problem: CO2 as a resource among competitors for ecosystem tissue structures as competitive mechanisms is unknown, rapid skeletal dominance. Phil. Trans. R. Soc. B Biol. Sci. 368, 20120442. growth, which can be used by scleractinians in competitive overgrowth Cornwall, C.E., Hepburn, C.D., Pritchard, D., Currie, K.I., McGraw, C.M., Hunter, K.A., Hurd, C.L., 2012. Carbon-use strategies in macroalgae: differential responses to and shading, can amount to 13–30% of the daily energy expenditures of lowered pH and implications for ocean acidification. J. Phycol. 48, 137–144. shallow water corals (Allemand et al., 2011, calculated from Edmunds Dai, C.F., 1990. Interspecific competition in Taiwanese corals with special reference to and Davies, 1986); and these costs are likely to be elevated under OA interactions between alcyonaceans and scleractinians. Mar. Ecol. Prog. Ser. 60, 291–297. conditions (McCulloch et al., 2012; Comeau et al., 2014). Diaz-Pulido, G., Gouezo, M., Tilbrook, B., Dove, S., Anthony, K.R.N., 2011. High CO2 Overall, our results show that aquarium-reared G. fascicularis alter enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156–162. the speed of deployment of mesenterial filaments, but not their ultimate Dickson, A.G., Sabine, C.L., Christian, J.R., 2007. Guide to Best Practices for CO2 Measurements (PICES Special Publication, 3). consequence, in coral-coral competition undertaken at high pCO2. Dove, S.G., Kline, D.I., Pantos, O., Angly, F.E., Tyson, G.W., Hoegh-Guldberg, O., 2013.

These findings indicate that physiological responses of corals to ele- Future reef decalcification under a business-as-usual CO2 emission scenario. Proc. Natl. Acad. Sci. U. S. A. 110, 15342–15347. vated pCO2 alone, may not suffice to predict the demographic perfor- fi Edmunds, P.J., Davies, P.S., 1986. An energy budget for Porites porites (Scleractinia). Mar. mances of corals to ocean acidi cation. As we report here, for example, Biol. 92, 339–347. G. fascicularis shows reduced skeletal growth under elevated pCO2, but Edmunds, P.J., Comeau, S., Lantz, C., Andersson, A., Briggs, C., Cohen, A., Gattuso, J.-P., maintains their competitive ability (see also Horwitz et al., 2017). Grady, J.M., Gross, K., Johnson, M., Muller, E.B., Ries, J.B., Tambutté, S., Tambutté, fi E., Venn, A., Carpenter, R.C., 2016. Integrating the effects of ocean acidification Furthermore, the calci cation rate of the coral Pocillopora verrucosa across functional scales on tropical coral reefs. Bioscience 66, 350–362. responds in different ways to elevated pCO2 depending on whether Evensen, N.R., Edmunds, P.J., 2016. Interactive effects of ocean acidification and colonies are engaged in coral-coral competition, or are spatially isolated neighboring corals on the growth of Pocillopora verrucosa. Mar. Biol. 163, 148. fi ff from other corals. While calcification of isolated colonies of P. verrucosa Evensen, N.R., Edmunds, P.J., 2017. Conspeci c aggregations mitigate the e ects of ocean acidification on calcification of the coral Pocillopora verrucosa. J. Exp. Biol. μ ff is depressed by high pCO2 (1033 to 1188 atm), it is una ected by si- 220, 1097–1105. milar seawater pCO2 conditions when colonies are engaged in in- Fabricius, K.E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De'ath, G., Okazaki, traspecific- (Evensen and Edmunds, 2016, 2017) or interspecific- R., Muehllehner, N., Glas, M.S., Lought, J.M., 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Chang. 1, (Horwitz et al., 2017) competition. Species interactions among scler- 165–169. actinian corals play a strong role in structuring coral communities Gaylord, B., Kroeker, K.J., Sunday, J.M., Anderson, K.M., Barry, J.P., Brown, N.E., (Lang and Chornesky, 1990), and thus, evaluating whether the com- Connell, S.D., Dupont, S., Fabricius, K.E., Hall-Spencer, J.M., Thiyagarajan, T.V., Vaughan, M.L.H., Widdicombe, S., Harley, C.D.G., 2015. Ocean acidification through petitive abilities of corals interact with the responses to elevated pCO2, the lens of ecological theory. Ecology 96, 3–15. is likely to improve predictions of how ocean acidification will affect Goreau, T.F., Goreau, N.J., Yonge, C.M., 1971. Reef corals: autotrophs or heterotrophs? coral communities. Biol. Bull. 141, 247–260. 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