Coral Reefs

, Volume 36, Issue 3, pp 947–956 | Cite as

Expansion of corals on temperate reefs: direct and indirect effects of marine heatwaves

  • C. A. Tuckett
  • T. de Bettignies
  • J. Fromont
  • T. Wernberg
Report

Abstract

Globally, many temperate marine communities have experienced significant temperature increases over recent decades in the form of gradual warming and heatwaves. As a result, these communities are shifting towards increasingly subtropical and tropical species compositions. Expanding coral populations have been reported from several temperate reef ecosystems along warming coastlines; these changes have been attributed to direct effects of gradual warming over decades. In contrast, increases in coral populations following shorter-term extreme warming events have rarely been documented. In this study, we compared coral populations on 17 temperate reefs in Western Australia before (2005/06) and after (2013) multiple marine heatwaves (2010–2012) affected the entire coastline. We hypothesised that coral communities would expand and change as a consequence of increasing local populations and recruitment of warm-affinity species. We found differences in coral community structure over time, driven primarily by a fourfold increase of one local species, Plesiastrea versipora, rather than recruitment of warm-affinity species. Coral populations became strongly dominated by small size classes, indicative of recent increased recruitment or recruit survival. These changes were likely facilitated by competitive release of corals from dominant temperate seaweeds, which perished during the heatwaves, rather than driven by direct temperature effects. Overall, as corals are inherently warm-water taxa not commonly associated with seaweed-dominated temperate reefs, these findings are consistent with a net tropicalisation. Our study draws attention to processes other than gradual warming that also influence the trajectory of temperate reefs in a changing ocean.

Keywords

Tropicalisation Kelp forests Seaweed decline High-latitude corals Plesiastrea versipora 

Supplementary material

338_2017_1586_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 21 kb)

References

  1. Abdo DA, Bellchambers LM, Evans SN (2012) Turning up the heat: increasing temperature and coral bleaching at the high latitude coral reefs of the Houtman Abrolhos Islands. PLoS ONE 7:e43878CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER-E Ltd., PlymouthGoogle Scholar
  3. Baird AH, Sommer B, Madin JS (2012) Pole-ward range expansion of Acropora spp. along the east coast of Australia. Coral Reefs 31:1063CrossRefGoogle Scholar
  4. Bassim KM, Sammarco PW (2003) Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diplora strigosa). Mar Biol 142:241–252CrossRefGoogle Scholar
  5. Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ (2015) Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol Lett 18:714–723CrossRefPubMedGoogle Scholar
  6. Bennett S, Wernberg T, Connell SD, Hobday AJ, Johnson CR, Poloczanska ES (2016) The ‘Great Southern Reef’: social, ecological and economic value of Australia’s neglected kelp forests. Mar Freshw Res 67:47–56CrossRefGoogle Scholar
  7. Burgess SN, McCulloch MT, Mortimer GE, Ward TM (2009) Structure and growth rates of the high-latitude coral Plesiastrea versipora. Coral Reefs 28:1005–1015CrossRefGoogle Scholar
  8. Carricart-Ganivet JP (2004) Sea surface temperature and the growth of the west Atlantic reef-building coral Montastraea annularis. J Exp Mar Biol Ecol 302:249–260CrossRefGoogle Scholar
  9. Coyer JA, Ambrose RF, Engle JM, Carroll JC (1993) Interactions between corals and algae on a temperate zone rocky reef: mediation by sea urchins. J Exp Mar Biol Ecol 167:21–37CrossRefGoogle Scholar
  10. Denis V, Mezaki T, Tanaka K, Kuo CY, De Palmas S, Keshavmurthy S, Chen CA (2013) Coverage, diversity, and functionality of a high-latitude coral community (Tatsukushi, Shikoku Island, Japan). PLoS ONE 8:e54330CrossRefPubMedPubMedCentralGoogle Scholar
  11. Denis V, Ribas-Deulofeu L, Loubeyres M, De Palmas S, Hwang S-J, Woo S, Song J-I, Chen CA (2014) Recruitment of the subtropical coral Alveopora japonica in the temperate waters of Jeju Island, South Korea. Bull Mar Sci 91:85–96CrossRefGoogle Scholar
  12. Edmunds PJ, Gates RD, Gleason DF (2001) The biology of larvae from the reef coral Porites asteroides and their response to temperature disturbances. Mar Biol 139:981–989CrossRefGoogle Scholar
  13. Foster T, Short JA, Falter JL, Ross C, McCulloch MT (2014) Reduced calcification in Western Australian corals during anomalously high summer water temperatures. J Exp Mar Biol Ecol 461:133–143CrossRefGoogle Scholar
  14. Fromont J, Hass C, Marsh L, Moore G, Salotti M, Titelius M, Whisson C (2006) Biodiversity of marine fauna on the Central West Coast, SRFME final milestone report—December 2006. Western Australian Museum, Perth, WAGoogle Scholar
  15. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103CrossRefGoogle Scholar
  16. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227CrossRefPubMedGoogle Scholar
  17. Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539CrossRefGoogle Scholar
  18. Greenstein BJ, Pandolfi JM (2008) Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Glob Chang Biol 14:513–528CrossRefGoogle Scholar
  19. Harrison PL, Dalton SJ, Carroll AG (2011) Extensive coral bleaching on the world’s southernmost coral reef at Lord Howe Island, Australia. Coral Reefs 30:775CrossRefGoogle Scholar
  20. Heyward AJ, Negri AP (2010) Plasticity of larval pre-competency in response to temperature: observations on multiple broadcast spawning coral species. Coral Reefs 29:631–636CrossRefGoogle Scholar
  21. Hobday AJ, Pecl GT (2013) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24:415–425CrossRefGoogle Scholar
  22. Hobday AJ, Alexander LV, Perkins SE, Smale DA, Straub SC, Oliver ECJ, Benthuysen JA, Burrows MT, Donat MG, Feng M, Holbrook NJ, Moore PJ, Scannell HA, Sen Gupta A, Wernberg T (2016) A hierarchical approach to defining marine heatwaves. Prog Oceanogr 141:227–238CrossRefGoogle Scholar
  23. Keith SA, Woolsey ES, Madin JS, Byrne M, Baird AH (2015) Differential establishment potential of species predicts a shift in coral assemblage structure across a biogeographic barrier. Ecography 38:1225–1234CrossRefGoogle Scholar
  24. Kersting DK, Bensoussan N, Linares C (2013) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8:e70820CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lafratta A, Fromont J, Speare P, Schönberg CHL (2016) Coral bleaching in turbid waters of north-western Australia. Mar Freshw Res 68:65–75Google Scholar
  26. Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeog 20:58–72CrossRefGoogle Scholar
  27. Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243CrossRefPubMedGoogle Scholar
  28. Markey KL, Abdo DA, Evans SN, Bosserelle C (2016) Keeping it local: dispersal limitations of coral larvae to the high latitude coral reefs of the Houtman Abrolhos Islands. PLoS ONE 11:e0147628CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mezaki T, Kubota S (2012) Changes of hermatypic coral community in coastal sea area of Kochi, high-latitude, Japan. Aquabiology 201:332–337Google Scholar
  30. Miller MW, Hay ME (1996) Coral–seaweed–grazer–nutrient interactions on temperate reefs. Ecol Monogr 66:323–344CrossRefGoogle Scholar
  31. Mizerek TL, Baird AH, Beaumont LJ, Madin JS (2016) Environmental tolerance governs the presence of reef corals at latitudes beyond reef growth. Glob Ecol Biogeogr 25:979–987CrossRefGoogle Scholar
  32. Moore JA, Bellchambers LM, Depczynski MR, Evans RD, Evans SN, Field SN, Friedman KJ, Gilmour JP, Holmes TH, Middlebrook R, Radford BT, Ridgway T, Shedrawi G, Taylor H, Thomson DP, Wilson SK (2012) Unprecedented mass bleaching and loss of coral across 12 degrees of latitude in Western Australia in 2010–11. PLoS ONE 7:e51807CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nakamura Y, Feary DA, Kanda M, Yamaoka K (2013) Tropical fishes dominate temperate reef fish communities within western Japan. PLoS ONE 8:e81107CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nozawa Y, Harrison PL (2000) Larval settlement patterns, dispersal potential, and the effect of temperature on settlement of larvae of the reef coral, Platygyra daedalea, from the Great Barrier Reef. In: Proceedings of the 9th international coral reef symposium, vol 1, pp 409–416Google Scholar
  35. Nozawa Y, Harrison PL (2007) Effects of elevated temperature on larval settlement and post-settlement survival in scleractinian corals, Acropora solitaryensis and Favites chinensis. Mar Biol 152:1181–1185CrossRefGoogle Scholar
  36. Pearce A, Feng M (2013) The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011. J Mar Syst 111–112:139–156CrossRefGoogle Scholar
  37. Pearce A, Lenanton R, Jackson G, Moore J, Feng M, Gaughan D (2011) The “marine heat wave” off Western Australia during the summer of 2010/11. Fisheries research report no. 222, Department of Fisheries, Perth, Western AustraliaGoogle Scholar
  38. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefPubMedGoogle Scholar
  39. Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925CrossRefGoogle Scholar
  40. Precht WF, Aronson RB (2004) Climate flickers and range shifts of reef corals. Front Ecol Environ 2:307–314CrossRefGoogle Scholar
  41. Randall CJ, Szmant AM (2009) Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28:537–545CrossRefGoogle Scholar
  42. Richards Z, Kirkendale L, Moore G, Hosie A, Huisman J, Bryce M, Marsh L, Bryce C, Hara A, Wilson N, Morrison S, Gomez O, Ritchie J, Whisson C, Allen M, Betterridge L, Wood C, Morrison H, Salotti M, Hansen G, Slack-Smith S, Fromont J (2016) Marine biodiversity in temperate Western Australia: multi-taxon surveys of Minden and Roe Reefs. Diversity 8:7CrossRefGoogle Scholar
  43. Rodolfo-Metalpa R, Richard C, Allemand D, Ferrier-Pages C (2006) Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures. J Exp Biol 209:4546–4556CrossRefPubMedGoogle Scholar
  44. Ross C, Ritson-Williams R, Olsen K, Paul VJ (2013) Short-term and latent post-settlement effects associated with elevated temperature and oxidative stress on larvae from the coral Porites astreoides. Coral Reefs 32:71–79CrossRefGoogle Scholar
  45. Schiel DR, Foster MS (1986) The structure of subtidal algal stands in temperate waters. Oceanogr Mar Biol Annu Rev 24:265–307Google Scholar
  46. Serrano E, Coma R, Ribes M (2012) A phase shift from macroalgal to coral dominance in the Mediterranean. Coral Reefs 31:1199CrossRefGoogle Scholar
  47. Serrano E, Coma R, Ribes M, Weitzmann B, Garcia M, Ballesteros E (2013) Rapid northward spread of a zooxanthellate coral enhanced by artificial structures and sea warming in the western Mediterranean. PLoS ONE 8:e52739CrossRefPubMedPubMedCentralGoogle Scholar
  48. Smale DA, Wernberg T (2012) Ecological observations associated with an anomalous warming event at the Houtman Abrolhos Islands, Western Australia. Coral Reefs 31:441CrossRefGoogle Scholar
  49. Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc R Soc Lond B Biol Sci 280:20122829CrossRefGoogle Scholar
  50. Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000–1009CrossRefPubMedGoogle Scholar
  51. Steneck RS, Johnson CR (2013) Kelp forests: dynamic patterns, processes and feedbacks. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer Associates, Sunderland, pp 315–336Google Scholar
  52. Sturges HA (1926) The choice of a class interval. J Am Stat Assoc 21:65–66CrossRefGoogle Scholar
  53. Thomson DP (2010) Range extension of the hard coral Goniopora norfolkensis (Veron & Pichon 1982) to the south-east Indian Ocean. J R Soc West Aust 93:81–83Google Scholar
  54. Thomson DP, Bearham D, Graham F, Eagle JV (2011) High latitude, deeper water coral bleaching at Rottnest Island, Western Australia. Coral Reefs 30:1107CrossRefGoogle Scholar
  55. Thomson DP, Babcock RC, Vanderklift MA, Symonds G, Gunson JR (2012) Evidence for persistent patch structure on temperate reefs and multiple hypotheses for their creation and maintenance. Estuar Coast Shelf Sci 96:105–113Google Scholar
  56. Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, Berghe EV, Worm B (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466:1098–1101CrossRefPubMedGoogle Scholar
  57. Vergés A, Tomas F, Cebrian E, Ballesteros E, Kizilkaya Z, Dendrinos P, Karamanlidis AA, Spiegel D, Sala E (2014a) Tropical rabbitfish and the deforestation of a warming temperate sea. J Ecol 102:1518–1527CrossRefGoogle Scholar
  58. Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E, Heck KL Jr, Booth DJ, Coleman MA, Feary DA, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Gupta AS, Smale DA, Tomas F, Wernberg T, Wilson SK (2014b) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc Lond B Biol Sci 281:20140846CrossRefGoogle Scholar
  59. Veron JEN (1993) Corals of Australia and the Indo-Pacific. University of Hawaii Press, HonoluluGoogle Scholar
  60. Veron JEN (2000) Corals of the world, vol 1–3. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  61. Veron JEN, Marsh LM (1988) Hermatypic corals of Western Australia. Records and annotated species list. Supplement. Rec West Aust Mus 29:1–136Google Scholar
  62. Vieira C, Keshavmurthy S, Ju S-J, Hyeong K, Seo I, Kang C-K, Hong H-K, Chen CA, Choi K-S (2016) Population dynamics of a high-latitude coral Alveopora japonica Eguchi from Jeju Island, off the southern coast of Korea. Mar Freshw Res 67:594–604CrossRefGoogle Scholar
  63. Wernberg T, de Bettignies T, Bijo AJ, Finnegan P (2016a) Physiological responses of habitat-forming seaweeds to increasing temperatures. Limnol Oceanogr 61:2180–2190CrossRefGoogle Scholar
  64. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013a) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78–82CrossRefGoogle Scholar
  65. Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Campbell A, Coleman MA, Steinberg PD, Kendrick GA, Connell SD (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400:7–16CrossRefGoogle Scholar
  66. Wernberg T, Thomsen MS, Connell SD, Russell BD, Waters JM, Zuccarello GC, Kraft GT, Sanderson C, West JA, Gurgel CFD (2013b) The footprint of continental-scale ocean currents on the biogeography of seaweeds. PLoS ONE 8:e80168CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (2016b) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172CrossRefPubMedGoogle Scholar
  68. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112CrossRefGoogle Scholar
  69. Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett 38:L04601CrossRefGoogle Scholar
  70. Yara Y, Oshima K, Yamanaka Y, Fujii M, Yamano H, Okada N (2011) Projection and uncertainty of the poleward range expansion of coral habitats in response to sea surface temperature warming: a multiple climate model study. Galaxea 13:11–20CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.School of Biological Sciences, UWA Oceans InstituteThe University of Western AustraliaCrawleyAustralia
  2. 2.UMS 2006 Patrimoine NaturelMuséum National d’Histoire NaturelleParisFrance
  3. 3.Western Australian MuseumWelshpool DCAustralia

Personalised recommendations