Advertisement

Coral Reefs

, Volume 34, Issue 4, pp 1243–1253 | Cite as

Adaptation to local thermal regimes by crustose coralline algae does not affect rates of recruitment in coral larvae

  • Nachshon SiboniEmail author
  • David Abrego
  • Christian Evenhuis
  • Murray Logan
  • Cherie A. Motti
Report

Abstract

Crustose coralline algae (CCA) are well known for their ability to induce settlement in coral larvae. While their wide distribution spans reefs that differ substantially in temperature regimes, the extent of local adaptation to these regimes and the impact they have on CCA inductive ability are unknown. CCA Porolithon onkodes from Heron (southern) and Lizard (northern) islands on Australia’s Great Barrier Reef (separated by 1181 km) were experimentally exposed to acute or prolonged thermal stress events and their thermal tolerance and recruitment capacity determined. A sudden onset bleaching model was developed to determine the health status of CCA based on the rate of change in the CCA live surface area (LSA). The interaction between location and temperature was significant (F (2,119) = 6.74, p = 0.0017), indicating that thermally driven local adaptation had occurred. The southern population remained healthy after prolonged exposure to 28 °C and exhibited growth compared to the northern population (p = 0.022), with its optimum temperature determined to be slightly below 28 °C. As expected, at the higher temperatures (30 and 32 °C) the Lizard Island population performed better that those from Heron Island, with an optimum temperature of 30 °C. Lizard Island CCA displayed the lowest bleaching rates at 30 °C, while levels consistently increased with temperature in their southern counterparts. The ability of those CCA deemed thermally tolerant (based on LSA) to induce Acropora millepora larval settlement was then assessed. While spatial differences influenced the health and bleaching levels of P. onkodes during prolonged and acute thermal exposure, thermally tolerant fragments, regardless of location, induced similar rates of coral larval settlement. This confirmed that recent thermal history does not influence the ability of CCA to induce settlement of A. millepora larvae.

Keywords

Crustose coralline algae Coral Settlement Thermal stress Bleaching Sudden onset bleaching model 

Notes

Acknowledgments

Funding was provided by the Australian Institute of Marine Science, Futures Project, Appropriation Fund 2233.

Supplementary material

338_2015_1346_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1321 kb)
338_2015_1346_MOESM2_ESM.docx (133 kb)
Supplementary material 2 (DOCX 132 kb)
338_2015_1346_MOESM3_ESM.docx (274 kb)
Supplementary material 3 (DOCX 274 kb)
338_2015_1346_MOESM4_ESM.docx (196 kb)
Supplementary material 4 (DOCX 195 kb)
338_2015_1346_MOESM5_ESM.docx (322 kb)
Supplementary material 5 (DOCX 321 kb)
338_2015_1346_MOESM6_ESM.docx (131 kb)
Supplementary material 6 (DOCX 130 kb)
338_2015_1346_MOESM7_ESM.docx (207 kb)
Supplementary material 7 (DOCX 206 kb)
338_2015_1346_MOESM8_ESM.docx (19 kb)
Supplementary material 8 (DOCX 19 kb)

References

  1. Adey WH (1998) Review—coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406CrossRefGoogle Scholar
  2. Albright R, Langdon C (2011) Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob Chang Biol 17:2478–2487CrossRefGoogle Scholar
  3. Albright R, Mason B (2013) Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLoS One 8:e56468PubMedCentralCrossRefPubMedGoogle Scholar
  4. Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446PubMedCentralCrossRefPubMedGoogle Scholar
  5. Berkelmans R (2002) Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar Ecol Prog Ser 229:73–82CrossRefGoogle Scholar
  6. Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83CrossRefGoogle Scholar
  7. Comeau S, Carpenter RC, Edmunds PJ (2014) Effects of irradiance on the response of the coral Acropora pulchra and the calcifying alga Hydrolithon reinboldii to temperature elevation and ocean acidification. J Exp Mar Bio Ecol 453:28–35CrossRefGoogle Scholar
  8. Committee on the Development of an Integrated Science Strategy for Ocean Acidification Monitoring Research, and Impacts Assessment, National Research Council (2010) Ocean acidification: a national strategy to meet the challenges of a changing ocean. The National Academies Press, Washington, D.C.Google Scholar
  9. Doropoulos C, Diaz-Pulido G (2013) High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae. Mar Ecol Prog Ser 475:93–99CrossRefGoogle Scholar
  10. Doropoulos C, Ward S, Diaz-Pulido G, Hoegh-Guldberg O, Mumby PJ (2012) Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol Lett 15:338–346CrossRefPubMedGoogle Scholar
  11. Fabricius K, De’Ath G (2001) Environmental factors associated with the spatial distribution of crustose coralline algae on the Great Barrier Reef. Coral Reefs 19:303–309CrossRefGoogle Scholar
  12. Fabricius K, De’ath G, Noonan S, Uthicke S (2014) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc R Soc Lond B Biol Sci 281:20132479CrossRefGoogle Scholar
  13. 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 Chang 1:165–169CrossRefGoogle Scholar
  14. Gilbert JA, Hill R, Doblin MA, Ralph PJ (2012) Microbial consortia increase thermal tolerance of corals. Mar Biol 159:1763–1771CrossRefGoogle Scholar
  15. Harrington L (2004) Ecology of crustose coralline algae: interactions with scleractinian corals and responses to environmental conditions. PhD thesis, James Cook University, Townsville, AustraliaGoogle Scholar
  16. Harrington L, Fabricius K, De’Ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437CrossRefGoogle Scholar
  17. Harvey A, Phillips L, Woelkerling W, Millar AJ (2006) The Corallinaceae, subfamily Mastophoroideae (Corallinales, Rhodophyta) in south-eastern Australia. Aust System Bot 19:387–429CrossRefGoogle Scholar
  18. Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279CrossRefGoogle Scholar
  19. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528CrossRefPubMedGoogle Scholar
  20. Howells EJ, Berkelmans R, van Oppen MJ, Willis BL, Bay LK (2013) Historical thermal regimes define limits to coral acclimatization. Ecology 94:1078–1088CrossRefPubMedGoogle Scholar
  21. Howells E, Beltran V, Larsen N, Bay L, Willis B, Van Oppen M (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120CrossRefGoogle Scholar
  22. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  23. Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642CrossRefPubMedGoogle Scholar
  24. Huisman JM, Leliaert F, Verbruggen H, Townsend RA (2009) Marine benthic plants of Western Australia’s shelf-edge atolls. Rec West Aus Mus 77:50–87Google Scholar
  25. Irving AD, Connell SD, Elsdon TS (2004) Effects of kelp canopies on bleaching and photosynthetic activity of encrusting coralline algae. J Exp Mar Bio Ecol 310:1–12CrossRefGoogle Scholar
  26. Johnson MD, Carpenter RC (2012) Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J Exp Mar Bio Ecol 434:94–101CrossRefGoogle Scholar
  27. Kennedy EV, Perry CT, Halloran PR, Iglesias-Prieto R, Schönberg CH, Wisshak M, Form AU, Carricart-Ganivet JP, Fine M, Eakin CM (2013) Avoiding coral reef functional collapse requires local and global action. Curr Biol 23:912–918CrossRefPubMedGoogle Scholar
  28. Kleypas JA, Danabasoglu G, Lough JM (2008) Potential role of the ocean thermostat in determining regional differences in coral reef bleaching events. Geophys Res Lett 35:L03613Google Scholar
  29. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117CrossRefGoogle Scholar
  30. Latham H (2008) Temperature stress-induced bleaching of the coralline alga Corallina officinalis: a role for the enzyme bromoperoxidase. Biosci Horizons 1:104–113CrossRefGoogle Scholar
  31. Limpert E, Stahel WA, Abbt M (2001) Log-normal distributions across the sciences: keys and clues. BioScience 51:341–352CrossRefGoogle Scholar
  32. Littler MM, Littler DS (1984) Models of tropical reef biogenesis: the contribution of algae. Prog Phycol Res 3:323–364Google Scholar
  33. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Chang Biol 15:2089–2100CrossRefGoogle Scholar
  34. Miller I, Logan M, Johns K, Jonker M, Osborne K, Sweatman H (2013) Determining background levels and defining outbreaks of crustose coralline algae disease on the Great Barrier Reef. Mar Freshw Res 64:1022–1028CrossRefGoogle Scholar
  35. Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Bio Ecol 116:193–217CrossRefGoogle Scholar
  36. Morse ANC, Iwao K, Baba M, Shimoike K, Hayashibara T, Omori M (1996) An ancient chemosensory mechanism brings new life to coral reefs. Biol Bull 191:149–154CrossRefGoogle Scholar
  37. Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131CrossRefGoogle Scholar
  38. Oliver T, Palumbi S (2011) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250CrossRefGoogle Scholar
  39. Ordoñez A, Doropoulos C, Diaz-Pulido G (2014) Effects of ocean acidification on population dynamics and community structure of crustose coralline algae. Biol Bull 226:255–268PubMedGoogle Scholar
  40. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New YorkCrossRefGoogle Scholar
  41. Price N (2010) Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 163:747–758PubMedCentralCrossRefPubMedGoogle Scholar
  42. Putnam HM, Edmunds PJ, Fan T-Y (2008) Effect of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biol Bull 215:135–142CrossRefPubMedGoogle Scholar
  43. Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society Special Report, London, pp 1–60Google Scholar
  44. Ritson-Williams R, Arnold S, Paul V, Steneck R (2014) Larval settlement preferences of Acropora palmata and Montastraea faveolata in response to diverse red algae. Coral Reefs 33:59–66CrossRefGoogle Scholar
  45. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  46. Siboni N, Abrego D, Motti CA, Tebben J, Harder T (2014) Gene expression patterns during the early stages of chemically induced larval metamorphosis and settlement of the coral Acropora millepora. PLoS One 9:e91082PubMedCentralCrossRefPubMedGoogle Scholar
  47. Siboni N, Abrego D, Seneca F, Motti CA, Andreakis N, Tebben J, Blackall LL, Harder T (2012) Using bacterial extract along with differential gene expression in Acropora millepora larvae to decouple the processes of attachment and metamorphosis. PLoS One 7:e37774PubMedCentralCrossRefPubMedGoogle Scholar
  48. Sinutok S, Hill R, Kühl M, Doblin MA, Ralph PJ (2014) Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis. Mar Biol 161:2143–2154CrossRefGoogle Scholar
  49. Smith-Keune C, van Oppen M (2006) Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef. Coral Reefs 25:493–502CrossRefGoogle Scholar
  50. Stanley SM, Ries JB, Hardie LA (2002) Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proc Natl Acad Sci U S A 99:15323–15326PubMedCentralCrossRefPubMedGoogle Scholar
  51. Steneck RS, Hacker SD, Dethier MN (1991) Mechanisms of competitive dominance between crustose coralline algae: an herbivore-mediated competitive reversal. Ecology 1991:938–950CrossRefGoogle Scholar
  52. Tebben J, Tapiolas DM, Motti CA, Abrego D, Negri AP, Blackall LL, Steinberg PD, Harder T (2011) Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a pseudoalteromonas bacterium. PLoS One 6:e19082PubMedCentralCrossRefPubMedGoogle Scholar
  53. Tebben J, Motti CA, Siboni N, Tapiolas DM, Negri AP, Schupp PJ, Kitamura M, Hatta M, Steinberg PD, Harder T (2015) Chemical mediation of coral larval settlement by crustose coralline algae. Sci Rep 5 doi: 10.1038/srep10803
  54. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163CrossRefGoogle Scholar
  55. Ulstrup KE, Berkelmans R, Ralph PJ, van Oppen MJH (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Mar Ecol Prog Ser 314:135–148CrossRefGoogle Scholar
  56. Underwood AJ, Keough MJ (2001) Supply-side ecology; the nature and consequences of variations in recruitment of intertidal organisms. In: Sunderland MA, Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, pp 183–200Google Scholar
  57. Vargas-Ángel B (2010) Crustose coralline algal diseases in the US-affiliated Pacific Islands. Coral Reefs 29:943–956CrossRefGoogle Scholar
  58. Webster NS, Soo R, Cobb R, Negri AP (2011) Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J 5:759–770PubMedCentralCrossRefPubMedGoogle Scholar
  59. Webster NS, Uthicke S, Botté ES, Flores F, Negri AP (2013) Ocean acidification reduces induction of coral settlement by crustose coralline algae. Glob Chang Biol 19:303–315PubMedCentralCrossRefPubMedGoogle Scholar
  60. Weeks S, Anthony K, Bakun A, Feldman G, Guldberg OH (2008) Improved predictions of coral bleaching using seasonal baselines and higher spatial resolution. Limnol Oceanogr 53:1369–1375CrossRefGoogle Scholar
  61. Weis VM (2010) The susceptibility and resilience of corals to thermal stress: adaptation, acclimatization or both? Mol Ecol 19:1515–1517CrossRefPubMedGoogle Scholar
  62. Whalan S, Webster NS, Negri AP (2012) Crustose coralline algae and a cnidarian neuropeptide trigger larval settlement in two coral reef sponges. PLoS One 7:e30386PubMedCentralCrossRefPubMedGoogle Scholar
  63. Whalan S, Abdul Wahab MA, Sprungala S, Poole AJ, de Nys R (2015) Larval settlement: the role of surface topography for sessile coral reef invertebrates. PLoS One 10:e0117675PubMedCentralCrossRefPubMedGoogle Scholar
  64. Williams D, Miller M, Kramer K (2008) Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705CrossRefGoogle Scholar
  65. Williams GJ, Price NN, Ushijima B, Aeby GS, Callahan S, Davy SK, Gove JM, Johnson MD, Knapp IS, Shore-Maggio A (2014) Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease. Proc R Soc Lond B Biol Sci 281:20133069CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Nachshon Siboni
    • 1
    • 2
    Email author
  • David Abrego
    • 1
    • 3
  • Christian Evenhuis
    • 2
  • Murray Logan
    • 1
  • Cherie A. Motti
    • 1
  1. 1.Australian Institute of Marine ScienceTownsvilleAustralia
  2. 2.University of TechnologySydneyAustralia
  3. 3.Zayed UniversityAbu DhabiUnited Arab Emirates

Personalised recommendations