Abstract
The physical and chemical environment around corals, as well as their physiology, can be affected by interactions with neighboring corals. This study employed small colonies (4 cm diameter) of Pocillopora verrucosa and Acropora hyacinthus configured in spatial arrays at 7 cm s−1 flow speed to test the hypothesis that ocean acidification (OA) alters interactions among them. Interaction effects were quantified for P. verrucosa using three measures of growth: calcification (i.e., weight), horizontal growth, and vertical growth. The study was carried out in May–June 2014 using corals from 10 m depth on the outer reef of Moorea, French Polynesia. Colonies of P. verrucosa were placed next to conspecifics or heterospecifics (A. hyacinthus) in arrangements of two or four colonies (pairs and aggregates) that were incubated at ambient and high pCO2 (~1000 µatm) for 28 days. There was an effect of pCO2, and arrangement type on multivariate growth (utilizing the three measures of growth), but no interaction between the main effects. Conversely, arrangement and pCO2 had an interactive effect on calcification, with an overall 23 % depression at high pCO2 versus ambient pCO2 (i.e., pooled among arrangements). Within arrangements, there was a 34–45 % decrease in calcification for solitary and paired conspecifics, but no effect in conspecific aggregates, heterospecific pairs, or heterospecific aggregates. Horizontal growth was negatively affected by pCO2 and arrangement type, while vertical growth was positively affected by arrangement type. Together, our results show that conspecific aggregations can mitigate the negative effects of OA on calcification of colonies within an aggregation.
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References
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth
Andersson AJ, Yeakel KL, Bates NR, de Putron SJ (2014) Partial offsets in ocean acidification from changing coral reef biogeochemistry. Nat Clim Change 4:56–61
Anthony KRN, Diaz-Pulido G, Verlinden N, Tilbrook B, Andersson AJ (2013) Benthic buffers and boosters of ocean acidification on coral reefs. Biogeosciences 10:4897–4909
Bonan GB (1988) The size structure of theoretical plant populations: spatial patterns and neighborhood effects. Ecology 69:1721–1730
Box SJ, Mumby PJ (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar Ecol Prog Ser 342:139–149
Bramanti L, Edmunds PJ (2016) Density-associated recruitment mediates coral population dynamics on a coral reef. Coral Reefs. doi:10.1007/s00338-016-1413-4
Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484
Chadwick NE, Morrow KM (2011) Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reef: an ecosystem in transition. Springer, Dordrecht, pp 347–371
Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc B 190:323–331
Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Change Biol 19:282–290
Chan NCS, Wangpraseurt D, Kühl M, Connolly SR (2016) Flow and coral morphology control coral surface pH: implications for the effects of ocean acidification. Front Mar Sci 3:10
Chevalier JP, Kühlmann DHH (1983) Les scléractiniaires de Moorea. Île de la Société (Polynésie Française). J de la Société des océanistes 77:55–75
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth
Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnol Oceanogr 160:1127–1134
Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014a) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnol Oceanogr 59:1081–1091
Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ (2014b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc B 281:20141339
Comeau S, Edmunds PJ, Lantz CA, Carpenter RC (2014c) Water flow modulates the response of coral reef communities to ocean acidification. Sci Rep 4:6681
Connell JH, Hughes TP, Wallace CC, Tanner JE, Harms KE, Kerr AM (2004) A long-term study of competition and diversity of corals. Ecol Monogr 74:179–210
Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc B Biol Sci 368:20120442. doi:10.1098/rstb.2012.0442
Cornell HV, Karlson RH (2000) Coral species richness: ecological versus biogeographical influences. Coral Reefs 19:37–49
Crossland CJ, Barnes DJ (1983) Dissolved nutrients and organic particulates in water flowing over coral reefs at Lizard Island. Aust J Mar Freshw Res 34:835–844
Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162
Dickson A, Sabine C, Christian J (2007) Guide to best practices for ocean CO2 measurement. In: Dickson A, Sabine C, Christian J (eds) PICES Special Publication 3
Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132
Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410
Edmunds PJ (2015) MCR LTER: coral reef: long-term population and community dynamics: corals, ongoing since 2005. knb-lter-mcr.4.33. doi:10.6073/pasta/1f05f1f52a2759dc096da9c24e88b1e8
Edmunds PJ, Leichter JJ, Johnston EC, Tong EJ, Toonen RJ (2016) Ecological and genetic variation in reef-building corals on four Society Islands. Limnol Oceanogr 61:543–557
Elahi R (2008) Effects of aggregation and species identity on the growth and behavior of mushroom corals. Coral Reefs 27:881–885
Evensen NR, Edmunds PJ, Sakai K (2015) Effects of pCO2 on spatial competition between the corals Montipora aequituberculata and massive Porites spp. Mar Ecol Prog Ser 541:123–134
Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169
Fine M, Loya Y (2003) Alternate coral–bryozoan competitive superiority during coral bleaching. Mar Biol 142:989–996
Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Dupont S, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PI, Russell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Ecol Evol Syst 41:127–147
Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17
Hurd CL (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J Phycol 51:599–605
Idjadi JA, Karlson RH (2007) Spatial arrangement of competitors influences coexistence of reef-building corals. Ecology 88:2449–2454
Jackson JBC, Buss L (1975) Allelopathy and spatial competition among coral reef invertebrates. Proc Natl Acad Sci USA 72:5160–5163
Jokiel P (1978) Effects of water motion on reef corals. J Exp Mar Biol Ecol 35:87–97
Karlson RH, Cornell HV, Hughes TP (2007) Aggregation influences coral species richness at multiple spatial scales. Ecology 88:170–177
Lang JC (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279
Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:1–16
Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Glob Biogeochem Cycles 14:639–654
Langdon C, Broecker WS, Hammond DE, Glenn E, Fitzsimmons K, Nelson SG, Peng TH, Hajdas I, Bonani G (2003) Effect of elevated CO2 on the community metabolism of an experimental coral reef. Glob Biogeochem Cycle 17:1011–1025
Lavigne H, Gattuso JP (2013) Seacarb: seawater carbonate chemistry with R, R package version 2.4.8. http://cran.r-project.org/web/packages/seacarb/index.html
Levas S, Grottoli AG, Warner ME, Cai WJ, Bauer J, Schoepf V, Baumann JH, Matsui Y, Gearing C, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y (2015) Organic carbon fluxes mediated by corals at elevated pCO2 and temperature. Mar Ecol Prog Ser 519:153–164
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and losers. Ecol Lett 4:122–131
Mack RN, Harper JL (1977) Interference in dune annuals: spatial pattern and neighborhood effects. J Ecol 65:345–363
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T, Meehl GA, Mitchell JFB, Nakicenovic N, Riahi K, Smith SJ, Stouffer RJ, Thomson AM, Weyant JP, Wilbanks TJ (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756
Moya A, Tambutté S, Tambutté E, Zoccola D, Caminiti N, Allemand D (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for “light enhanced calcification”. J Exp Biol 209:3413–3419
Mumby PJ, van Woesik R (2014) Consequences of ecological, evolutionary and biogeochemical uncertainty for coral reef responses to climatic stress. Curr Biol 24:413–423
Naumann MS, Haas A, Struck U, Mayr C, El-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29:649–659
Pratchett MS, McCowan DM, Maynard JA, Heron SF (2013) Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea French Polynesia. PLoS One 8:e70443
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Rasband WS (1997) ImageJ. National Institutes of Health, Bethesda
Reidenbach MA, Koseff JR, Monismith SG, Steinbuck JV, Genin A (2006) The effects of waves and morphology on mass transfer within branched reef corals. Limnol Oceanogr 51:1134–1141
Renegar DA, Blackwelder PL, Moulding AL (2008) Coral ultrastructural response to elevated pCO2 and nutrients during tissue repair and regeneration. In: Proceedings of the 11th international coral reef symposium, Ft. Lauderdale, Florida, vol 2, pp 1320–1324
Rinkevich B, Loya Y (1985) Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66:100–105
Romano SL (1990) Long-term effects of interspecific aggression on growth of the reef building corals Cyphastrea ocellina (Dana) and Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 140:135–146
Schoepf V, Grottoli AG, Warner ME, Cai WJ, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann JH (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8:e750469
Sebens KP, Witting J, Helmuth B (1997) The effects of water flow and branch spacing on particle capture by the reef coral Madracis mirabilis (Duchaissaing and Michelotti). J Exp Mar Biol Ecol 211:1–28
Shamberger KEF, Cohen AL, Golbuu Y, McCorkle DC, Lentz SJ, Barkley HC (2014) Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys Res Lett 41:499–504
Spencer-Davies P (1989) Short-term growth measurements of coral growth using an accurate buoyant weighing technique. Mar Biol 101:389–395
Stimson J, Kinzie RA III (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74
Stoll P, Prati D (2001) Intraspecific aggregation alters competitive interactions in experimental plant communities. Ecology 82:319–327
Stoll P, Weiner J (2000) A neighborhood view of interactions among plants. In: Dieckmann U, Law R, Metz JAJ (eds) The geometry of ecological interactions: simplifying spatial complexity. Cambridge University Press, Cambridge, pp 11–27
Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16
Veron J (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Washburn L (2015) MCR LTER: Coral Reef: Ocean Currents and Biogeochemistry: salinity, temperature and current at CTD and ADCP mooring FOR01 from 2004 ongoing. knb-lter-mcr.30.30. doi:10.6073/pasta/da2321da9139f3cba86e883c8f7a36a3
Wild C, Niggl W, Naumann MS, Haas AF (2010) Organic matter release by Red Sea coral reef organisms—potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411:61–71
Zilberberg C, Edmunds PJ (2001) Competition among small colonies of Agaricia: the importance of size asymmetry in determining competitive outcome. Mar Ecol Prog Ser 221:125–133
Acknowledgments
This research was supported by funding from the National Science Foundation (NSF) to the Moorea Coral Reef, Long-Term Ecological Research site (OCE 12-36905), NSF funding for OA research (OCE 10-41270 and OCE 14-15268), and gifts from the Gordon and Betty Moore Foundation. We are grateful to the staff at the Richard B. Gump South Pacific Research Station for hosting our visit to Moorea, to C. Lantz, V. Moriarty, M. Ho for field assistance in Moorea, and S. Comeau and C. Doropoulos for discussions that improved the quality of this work. We are also grateful to the reviewers for their help to improve the quality of the manuscript. This is contribution number 242 of the California State University, Northridge, Marine Biology Program.
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Evensen, N.R., Edmunds, P.J. Interactive effects of ocean acidification and neighboring corals on the growth of Pocillopora verrucosa . Mar Biol 163, 148 (2016). https://doi.org/10.1007/s00227-016-2921-z
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DOI: https://doi.org/10.1007/s00227-016-2921-z