Abstract
Coral colonies regularly suffer tissue damage from natural and anthropogenic sources. The resultant wounds can decrease colony fitness and act as sources of infection or algal overgrowth. By systematically breaking branches on 54 Pocillopora meandrina colonies and following in situ tissue regeneration (April–August 2017), variation in the wound recovery process was investigated within colonies, among colonies, and across four sites on O‘ahu, Hawai‘i. Ninety-five percent of all wounds healed, with an average healing time of 42 days. Average healing time was not different between initial and subsequent wounds. The relative importance of intrinsic factors, extrinsic factors, and disturbance history for the wound repair process was examined. Previous colony stressors, i.e., percent live coral tissue and bleaching history, were not correlated with wound healing time. These results indicate that wound repair is a priority for P. meandrina. Colony size and depth were significantly correlated with wound healing time: larger colonies healed 14 days faster than smaller colonies, and deeper colonies healed 25 days slower than shallower colonies. These findings support the hypothesis that larger colonies have more energy available for tissue regeneration. The observation of longer healing times for deeper colonies is likely driven by extrinsic factors that vary with depth, including temperature, wave energy, and irradiance. Overall, we show that wound healing in P. meandrina is physiologically resilient to previous stressors, but is affected by both colony size and depth. Understanding drivers of variation in regenerative processes for corals is critical for predicting coral population recovery after disturbances.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated during this study are provided in the electronic supplementary material.
References
Anderson KD, Cantin NE, Heron SF, Pisapia C, Morgan S (2017) Variation in growth rates of branching corals along Australia’s Great Barrier Reef. Sci Rep. https://doi.org/10.1038/s41598-017-03085-1
Bak RP, Steward-Van Es Y (1980) Regeneration of superficial damage in the scleractinian corals Agaricia agaricites f. purpurea and Porites astreoides. Bull Mar Sci 30:883–887
Bartoń K (2016) MuMIn: multi-model inference. R package version 1.15.6
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bégin C, Schelten CK, Nugues MM, Hawkins J, Roberts C, Cote IM (2016) Effects of protection and sediment stress on coral reefs in Saint Lucia. PLoS One 11:1–16. https://doi.org/10.1371/journal.pone.0146855
Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242. https://doi.org/10.1128/AEM.69.7.4236
Bonesso JL, Leggat W, Ainsworth TD (2017) Exposure to elevated sea-surface temperatures below the bleaching threshold impairs coral recovery and regeneration following injury. PeerJ. https://doi.org/10.7717/peerj.3719
Burmester EM, Finnerty JR, Kaufman L, Rotjan RD (2017) Temperature and symbiosis affect lesion recovery in experimentally wounded, facultatively symbiotic temperate corals. Mar Ecol Prog Ser 570:87–99
Burmester EM, Breef-Pilz A, Lawrence NF, Kaufman L, Finnerty JR, Rotjan RD (2018) The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals. Ecol Evol. https://doi.org/10.1002/ece3.4531
Cameron CM, Edmunds PJ (2014) Effects of simulated fish predation on small colonies of massive Porites spp. and Pocillopora meandrina. Mar Ecol Prog Ser 508:139–148. https://doi.org/10.3354/meps10862
Chang S, Iaccarino G, Ham F, Elkins C, Monismith S (2014) Local shear and mass transfer on individual coral colonies: computations in unidirectional and wave-driven flows. J Geophys Res Ocean. https://doi.org/10.1002/2013JC009751
Counsell CWW, Donahue MJ, Edwards KF, Franklin EC, Hixon MA (2018) Variation in coral-associated cryptofaunal communities across spatial scales and environmental gradients. Coral Reefs 37:827–840. https://doi.org/10.1007/s00338-018-1709-7
Croquer A, Villamizar E, Noriega N (2002) Environmental factors affecting tissue regeneration of the reef building coral Montastraea annularis (Faviidae) at Los Roques National Park, Venezuela. Rev Biol Trop 50:1055–1065
Darling ES, Alvarez-filip L, Oliver TA, McClanahan TR, Cote IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386. https://doi.org/10.1111/j.1461-0248.2012.01861.x
Defilippo L, Burmester EM, Kaufman L, Rotjan RD (2016) Patterns of surface lesion recovery in the Northern Star Coral, Astrangia poculata. J Exp Mar Bio Ecol 481:15–24. https://doi.org/10.1016/j.jembe.2016.03.016
Dornelas M, Madin JS, Baird AH, Connolly SR (2017) Allometric growth in reef-building corals. Proc R Soc B Biol Sci 284:20170053
Edmunds PJ, Burgess SC (2016) Size-dependent physiological responses of the branching coral Pocillopora verrucosa to elevated temperature and pCO2. J Exp Biol 219:3896–3906. https://doi.org/10.1242/jeb.194753
Edmunds PJ, Burgess SC (2018) Colony size and turbulent flow speed modulate the calcification response of the coral Pocillopora verrucosa to temperature. Mar Biol 165:1–12. https://doi.org/10.1007/s00227-017-3257-z
Edmunds PJ, Yarid A (2017) The effects of ocean acidification on wound repair in the coral Porites spp. J Exp Mar Bio Ecol 486:98–104. https://doi.org/10.1016/j.jembe.2016.10.001
Elahi R, Edmunds PJ (2007) Tissue age affects calcification in the scleractinian coral Madracis mirabilis. Biol Bull 212:20–28. https://doi.org/10.2307/25066577
Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar Ecol Prog Ser 234:119–125
Fisher EM, Fauth JE, Hallock P, Woodley CM (2007) Lesion regeneration rates in reef-building corals Montastraea spp. as indicators of colony condition. Mar Ecol Prog Ser 339:61–71
Fong P, Lirman D (1995) Hurricanes cause population expansion of the branching coral Acropora palmata (Scleractinia): wound healing and growth patterns of asexual recruits. Mar Ecol 16:317–335
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks
Franklin EC, Jokiel PL, Donahue MJ (2013) Predictive modeling of coral distribution and abundance in the Hawaiian Islands. Mar Ecol Prog Ser 481:121–132. https://doi.org/10.3354/meps10252
Goldshmid R, Holzman R, Weihs D, Genin A (2004) Aeration of corals by sleep-swimming fish. Limnol Oceanogr 49:1832–1839. https://doi.org/10.4319/lo.2004.49.5.1832
Goreau T, Macfarlane A (1990) Reduced growth rate of Montastrea annularis following the 1987–1988 coral-bleaching event. Coral Reefs 8:211–215
Gove JM, Williams GJ, McManus MA, Clark SJ, Ehses JS, Wedding LM (2015) Coral reef benthic regimes exhibit non-linear threshold responses to natural physical drivers. Mar Ecol Prog Ser 522:33–48. https://doi.org/10.3354/meps11118
Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, Mcginley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833. https://doi.org/10.1111/gcb.12658
Hall VR (1997) Interspecific differences in the regeneration of artificial injuries on scleractinian corals. J Exp Mar Bio Ecol 212:9–23
Henry L-AA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals—a review. Int Rev Hydrobiol 90:125–158. https://doi.org/10.1002/iroh.200410759
Holbrook SJ, Brooks AJ, Schmitt RJ, Stewart HL (2008) Effects of sheltering fish on growth of their host corals. Mar Biol 155:521–530. https://doi.org/10.1007/s00227-008-1051-7
Hughes TP, Connell JH (1987) Population dynamics based on size or age? A reef-coral analysis. Am Nat 129:818–829
Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, Mcwilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018a) Global warming transforms coral reef assemblages. Nature 556:492–497. https://doi.org/10.1038/s41586-018-0041-2
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JA, Hoey AS, Hoogenboom M, Lowe RJ, Mcculloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018b) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359(6371):80–83. https://doi.org/10.1126/science.aan8048
Jayewardene D, Donahue MJ, Birkeland C (2009) Effects of frequent fish predation on corals in Hawaii. Coral Reefs 28:499–506. https://doi.org/10.1007/s00338-009-0475-y
Johnston EC, Forsman ZH, Toonen RJ (2018) A simple molecular technique for distinguishing species reveals frequent misidentification of Hawaiian corals in the genus Pocillopora. PeerJ 6:e4355. https://doi.org/10.7717/peerj.4355
Jokiel P, Coles S (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208
Kaniewska P, Anthony KRN, Hoegh-guldberg O (2008) Variation in colony geometry modulates internal light levels in branching corals, Acropora humilis and Stylophora pistillata. Mar Biol 155:649–660. https://doi.org/10.1007/s00227-008-1061-5
Kaniewska P, Magnusson SH, Anthony KRN, Reef R, Kuhl M, Hoegh-Guldberg O (2011) Importance of macro- versus microstructure in modulating light levels inside coral colonies. J Phycol 47:846–860. https://doi.org/10.1111/j.1529-8817.2011.01021.x
Kayal M, Vercelloni J, Wand MP, Adjeroud M (2015) Searching for the best bet in life-strategy: a quantitative approach to individual performance and population dynamics in reef-building corals. Ecol Complex 23:73–84. https://doi.org/10.1016/j.ecocom.2015.07.003
Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348. https://doi.org/10.1111/mec.12391
Kramarsky-Winter E, Loya Y (2000) Tissue regeneration in the coral Fungia granulosa: the effect of extrinsic and intrinsic factors. Mar Biol 137:867–873
Lenihan HS, Edmunds PJ (2010) Response of Pocillopora verrucosa to corallivory varies with environmental conditions. Mar Ecol Prog Ser 409:51–63. https://doi.org/10.3354/meps08595
Lester RT, Bak RP (1985) Effects of environment on regeneration rate of tissue lesions in the reef coral Montastrea annularis (Scleractinia). Mar Ecol Prog Ser 24:183–185
Levy O, Karako-Lampert S, Ben-Asher HW, Zoccola D, Page G, Ferrier-Pages C (2016) Molecular assessment of the effect of light and heterotrophy in the scleractinian coral Stylophora pistillata. Proc R Soc B 283:20153025. https://doi.org/10.1098/rspb.2015.3025
Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480. https://doi.org/10.1038/nature05328
Madin JS, Baird AH, Dornelas M, Connolly SR (2014) Mechanical vulnerability explains size-dependent mortality of reef corals. Ecol Lett 17:1008–1015. https://doi.org/10.1111/ele.12306
Madin JS, Hoogenboom MO, Connolly SR, Darling ES, Falster DS, Huang D, Keith SA, Mizerek T, Pandol JM, Putnam HM, Baird AH (2016) A trait-based approach to advance coral reef science. Trends Ecol Evol 31:419–428. https://doi.org/10.1016/j.tree.2016.02.012
Meesters EH, Bak RP (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. Mar Ecol Prog Ser 96:189–198
Meesters EH, Noordeloos M, Bak RP (1994) Damage and regeneration: links to growth in the reef-building coral Montastrea annularis. Mar Ecol Prog Ser 112:119–128. https://doi.org/10.3354/Meps112119
Meesters EH, Wesseling I, Bak RP (1996) Partial mortality in three species of reef-building corals and the relation with colony morphology. Bull Mar Sci 58:838–852
Meesters EH, Pauchli W, Bak RPM (1997) Predicting regeneration of physical damage on a reef-building coral by regeneration capacity and lesion shape. Mar Ecol Prog Ser 146:91–99
Nagelkerken I, Meesters E, Bak R (1999) Depth-related variation in regeneration of artificial lesions in the Caribbean corals Porites astreoides and Stephanocoenia michelinii. J Exp Mar Bio Ecol 234:29–39
Nakamura T (2010) Importance of water-flow on the physiological responses of reef-building corals. Galaxea, J Coral Reef Stud 12:1–14
Oren U, Benayahu Y, Loya Y (1997) Effect of lesion size and shape on regeneration of the Red Sea coral Favia favus. Mar Ecol Prog Ser 146:101–107. https://doi.org/10.3354/meps146101
Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Colony integration during regeneration in the stony coral Favia favus. Ecology 83:802–813. https://doi.org/10.2307/2680199
Osinga R, Schutter M, Griffioen B, Wijffels RH, Verreth JA, Shafir S, Henard S, Taruffi M, Gili C, Lavorano S (2011) The biology and economics of coral growth. Mar Biotechnol 13:658–671. https://doi.org/10.1007/s10126-011-9382-7
Piniak GA, Brown EK (2008) Growth and mortality of coral transplants (Pocillopora damicornis) along a range of sediment influence in Maui, Hawai‘i. Pacific Sci 62:39–55
Rinkevich B (1994) Do reproduction and regeneration in damaged corals compete for energy allocation? Mar Ecol Prog Ser 143:297–302
Rinkevich B, Loya Y (1989) Reproduction in regenerating colonies of the coral Stylophora pistilata. In: Spanier E, Steinberger Y, Luria M (eds) Environmental quality and ecosystem stability. ISEEQS Publications IVB, Jerusalem, pp 259–265
Rodríguez-Villalobos JC, Work TM, Calderon-Aguilera LE, Reyes-Bonilla H, Hernández L (2015) Explained and unexplained tissue loss in corals from the Tropical Eastern Pacific. Dis Aquat Organ 116:121–131. https://doi.org/10.3354/dao02914
Rodríguez-Villalobos JC, Work TM, Calderon-Aguilera LE (2016) Wound repair in Pocillopora. J Invertebr Pathol 139:1–5. https://doi.org/10.1016/j.jip.2016.07.002
Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91. https://doi.org/10.3354/meps07531
Rotjan RD, Dimond JL, Thornhill DJ, Leichter JJ, Helmuth B, Kemp DW, Lewis SM (2006) Chronic parrotfish grazing impedes coral recovery after bleaching. Coral Reefs 25:361–368. https://doi.org/10.1007/s00338-006-0120-y
Sabine AM, Smith TB, Williams DE, Brandt ME (2015) Environmental conditions influence tissue regeneration rates in scleractinian corals. Mar Pollut Bull 95:253–264. https://doi.org/10.1016/j.marpolbul.2015.04.006
Schoepf V, Grottoli G, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015) Annual coral bleaching and the long-term recovery capacity of coral. Proc R Soc B. https://doi.org/10.1098/rspb.2015.1887
Sebens K, Helmuth B, Carrington E, Aguis B (2003) Effects of water flow on growth and energetics of the scleractinian coral Agaricia tenuifolia in Belize. Coral Reefs 22:35–47. https://doi.org/10.1007/s00338-003-0277-6
Smith LW, Wirshing HH, Baker AC, Birkeland C (2008) Environmental versus genetic influences on growth rates of the corals Pocillopora eydouxi and Porites lobata. Pacific Sci 62:57–69. https://doi.org/10.2984/1534-6188(2008)62%5b57:evgiog%5d2.0.co;2
Stella JS, Jones GP, Pratchett MS (2010) Variation in the structure of epifaunal invertebrate assemblages among coral hosts. Coral Reefs 29:957–973. https://doi.org/10.1007/s00338-010-0648-8
Stewart HL, Holbrook SJ, Schmitt RJ, Brooks AJ (2006) Symbiotic crabs maintain coral health by clearing sediments. Coral Reefs 25:609–615. https://doi.org/10.1007/s00338-006-0132-7
Stier AC, Gil MA, McKeon CS, Lemer S, Leray M, Mills SC, Osenberg CW (2012) Housekeeping mutualisms: do more symbionts facilitate host performance? PLoS One 7:e32079. https://doi.org/10.1371/journal.pone.0032079
Tortolero-langarica JDJA, Rodríguez-troncoso AP, Cupul-Magaña AL, Carricart-Ganivet JP (2017) Calcification and growth rate recovery of the reef-building Pocillopora species in the northeast tropical Pacific following an ENSO disturbance. PeerJ. https://doi.org/10.7717/peerj.3191
Traylor-Knowles N (2016) Distinctive wound-healing characteristics in the corals Pocillopora damicornis and Acropora hyacinthus found in two different temperature regimes. Mar Biol 163:2–7. https://doi.org/10.1007/s00227-016-3011-y
van Woesik R (1998) Lesion healing on massive Porites spp. corals. MEPS 164:213–220. https://doi.org/10.3354/meps164213
Walsh KJE, Mcbride JL, Klotzbach PJ, Balachandran S, Camargo SJ, Holland G, Knutson TR, Kossin JP, Lee T, Sobel A, Sugi M (2016) Tropical cyclones and climate change. WIREs Clim Chang 7:65–89. https://doi.org/10.1002/wcc.371
Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453
Acknowledgements
J. Jones supported this project with boat and dive safety guidance. Fieldwork was conducted by C. Counsell, E. Johnston, T. Sale, D. Ford, and C. Schlieman. Both C. Counsell’s and E. Johnston’s participation in this study was supported by National Science Foundation Graduate Research Fellowships (Grant No. 2012103208 and 2015184863, respectively). Additional funding was provided by the Castle Foundation (Grant No. 3846, M Hixon PI). This is HIMB contribution No. 1771 and SOEST contribution No. 10810. We thank the three anonymous reviewers and the associate editor whose comments improved this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the sampling, care, and use of animals were followed and all necessary approvals were obtained. Sampling was completed under the HIMB Special Activity Permit 2018-3.
Additional information
Responsible Editor: D. Gochfeld.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by undisclosed experts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Counsell, C.W.W., Johnston, E.C. & Sale, T.L. Colony size and depth affect wound repair in a branching coral. Mar Biol 166, 148 (2019). https://doi.org/10.1007/s00227-019-3601-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-019-3601-6