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Coral Reefs

, Volume 37, Issue 1, pp 267–277 | Cite as

Long-term growth rates and effects of bleaching in Acropora hyacinthus

  • Zachary Gold
  • Stephen R. Palumbi
Report

Abstract

Understanding the response of coral growth to natural variation in the environment, as well as to acute temperature stress under current and future climate change conditions, is critical to predicting the future health of coral reef ecosystems. As such, ecological surveys are beginning to focus on corals that live in high thermal stress environments to understand how future coral populations may adapt to climate change. We investigated the relationship between coral growth, thermal microhabitat, symbionts type, and thermal acclimatization of four species of the Acropora hyacinthus complex in back-reef lagoons in American Samoa. Coral growth was measured from August 2010 to April 2016 using horizontal planar area of coral colonies derived from photographs and in situ maximum width measurements. Despite marked intraspecific variation, we found that planar colony growth rates were significantly different among cryptic species. The highly heat tolerant A. hyacinthus variant “HE” increased in area an average of 2.9% month−1 (0.03 cm average mean radial extension month−1). By contrast, the three less tolerant species averaged 6.1% (0.07 cm average mean radial extension month−1). Planar growth rates were 40% higher on average in corals harboring Clade C versus Clade D symbiont types, although marked inter-colony variation in growth rendered this difference nonsignificant. Planar growth rates for all four species dropped to near zero following a 2015 bleaching event, independent of the visually estimated percent area of bleaching. Within 1 yr, growth rates recovered to previous levels, confirming previous studies that found sublethal effects of thermal stress on coral growth. Long-term studies of individual coral colonies provide an important tool to measure impacts of environmental change and allow integration of coral physiology, genetics, symbionts, and microclimate on reef growth patterns.

Keywords

Coral growth Coral bleaching Acropora hyacinthus Symbiont Thermal stress American Samoa 

Notes

Acknowledgements

We acknowledge Megan Morikawa, Lupita Ruiz-Jones, Rachel Bay, Noah Rose, Nikki Traylor-Knowles, and Francois Seneca for assisting in data collection of coral growth measurements. We also thank the U.S. National Park of American Samoa for permission to work on Ofu reefs and Carlo Caruso for logistical and research help. Supported by the Gordon and Betty Moore Foundation, the National Science Foundation, the Flora Family Foundation, and Stanford University Vice Provost for Undergraduate Education. Lastly, we would like to thank Jesse Gomer for statistical and computational assistance.

Supplementary material

338_2018_1656_MOESM1_ESM.docx (383 kb)
Supplementary material 1 (DOCX 382 kb)

References

  1. Anderson KD, Heron SF, Pratchett MS (2015) Species-specific declines in the linear extension of branching corals at a subtropical reef, Lord Howe Island. Coral Reefs 34:479–490CrossRefGoogle Scholar
  2. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550CrossRefGoogle Scholar
  3. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  4. Bak RPM, Nieuwland G, Meesters EH (2009) Coral Growth Rates Revisited after 31 Years: What is Causing Lower Extension Rates in Acropora palmata? Bull Mar Sci 84:287–294Google Scholar
  5. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  6. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Coral reefs: corals’ adaptive response to climate change. Nature 430:741CrossRefPubMedGoogle Scholar
  7. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci 110:1387–1392CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting Linear Mixed-Effects Models using lme4Google Scholar
  9. Bay RA, Palumbi SR (2014) Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals. Curr Biol 24:2952–2956CrossRefPubMedGoogle Scholar
  10. Bay RA, Palumbi SR (2015) Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol Evol 7:1602–1612CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bay RA, Rose NH, Logan CA, Palumbi SR (2017) Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Sci Adv 3:e1701413CrossRefPubMedPubMedCentralGoogle Scholar
  12. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B Biol Sci 273:2305–2312CrossRefGoogle Scholar
  13. Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141CrossRefPubMedGoogle Scholar
  14. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic Divergence across Habitats in the Widespread Coral Seriatopora hystrix and Its Associated Symbiodinium. PLoS One 5:e10871CrossRefPubMedPubMedCentralGoogle Scholar
  15. Charuchinda M, Hylleberg J (2009) Skeletal extension of Acropora formosa at a fringing reef in the Andaman Sea. Coral Reefs 3:215–219CrossRefGoogle Scholar
  16. Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:1–6CrossRefGoogle Scholar
  17. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37CrossRefPubMedGoogle Scholar
  18. Edmunds PJ, Bruno JF, Carlon DB (2004) Effects of depth and microhabitat on growth and survivorship of juvenile corals in the Florida Keys. Mar Ecol Prog Ser 278:115–124CrossRefGoogle Scholar
  19. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution (N Y) 58:324–337Google Scholar
  20. Gillette P (2012) Genetic variation in thermal tolerance in the coral Pocillopora damicornis and its effects on growth, photosynthesis and survival. Univ Miami Master’s ThesisGoogle Scholar
  21. Grime JP, Hunt R (1975) Relative Growth-Rate: Its Range and Adaptive Significance in a Local Flora. J Ecol 63:393CrossRefGoogle Scholar
  22. Jones A, Berkelmans R (2010) Potential Costs of Acclimatization to a Warmer Climate: Growth of a Reef Coral with Heat Tolerant vs. Sensitive Symbiont Types. PLoS One 5:e10437CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jones AM, Berkelmans R (2011) Tradeoffs to Thermal Acclimation: Energetics and Reproduction of a Reef Coral with Heat Tolerant Symbiodinium Type-D. J Mar Biol 2011:1–12CrossRefGoogle Scholar
  24. Knowlton N, Weil E (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330CrossRefPubMedGoogle Scholar
  25. Ladner JT, Palumbi SR (2012) Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol Ecol 21:2224–2238CrossRefPubMedGoogle Scholar
  26. Linares C, Pratchett MS, Coker DJ (2011) Recolonisation of Acropora hyacinthus following climate-induced coral bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 438:97–104CrossRefGoogle Scholar
  27. Little AF, Van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494CrossRefPubMedGoogle Scholar
  28. Madin JS, Hughes TP, Connolly SR (2012) Calcification, Storm Damage and Population Resilience of Tabular Corals under Climate Change. PLoS One 7:e46637CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mendes JM, Woodley JD (2002) Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102CrossRefGoogle Scholar
  30. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One 4:e6364CrossRefPubMedPubMedCentralGoogle Scholar
  31. Morikawa M, Palumbi S (2018) Influence of genotype on coral growth (in prep.)Google Scholar
  32. Neal BP, Lin T-H, Winter RN, Treibitz T, Beijbom O, Kriegman D, Kline DI, Mitchell BG (2015) Methods and measurement variance for field estimations of coral colony planar area using underwater photographs and semi-automated image segmentation. Environ Monit Assess 187:1–11CrossRefGoogle Scholar
  33. Nelder JA, Baker RJ (2004) Generalized Linear Models. Encyclopedia of Statistical Sciences. John Wiley & Sons, Inc.Google Scholar
  34. Oliver T, Palumbi S (2009) Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser 378:93–103CrossRefGoogle Scholar
  35. Oliver TA, Palumbi SR (2011a) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250CrossRefGoogle Scholar
  36. Oliver TA, Palumbi SR (2011b) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440CrossRefGoogle Scholar
  37. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354CrossRefPubMedGoogle Scholar
  38. Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65CrossRefPubMedGoogle Scholar
  39. Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898CrossRefPubMedGoogle Scholar
  40. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2009) nlme: Linear and nonlinear mixed effects models. R Packag version 3:96Google Scholar
  42. Pinzon JH, LaJeunesse T (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325CrossRefPubMedGoogle Scholar
  43. Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci 110:3961–3966CrossRefPubMedPubMedCentralGoogle Scholar
  44. Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME, Coffroth MA (2014) Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Mol Ecol 23:3330–3340CrossRefPubMedGoogle Scholar
  45. Pratchett MS, Anderson KD, Hoogenboom MO, Widman E, Baird AH, Pandolfi JM, Edmunds PJ, Lough JM (2015) Spatial, temporal and taxonomic variation in coral growth—implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol An Annu Rev 53:215–295Google Scholar
  46. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc London B Biol Sci 272:573–579CrossRefGoogle Scholar
  47. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  48. Rose NH, Bay RA, Morikawa MK, Palumbi SR (2017) Polygenic evolution drives species divergence and climate adaptation in corals. Evolution (N Y)Google Scholar
  49. Rowan R (2004) Coral bleaching: Thermal adaptation in reef coral symbionts. Nature 430:742CrossRefPubMedGoogle Scholar
  50. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMedPubMedCentralGoogle Scholar
  51. Seneca FO, Palumbi SR (2015) The role of transcriptome resilience in resistance of corals to bleaching. Mol Ecol 24:1467–1484CrossRefPubMedGoogle Scholar
  52. Sheets B, Palumbi S (2018) Accurate connectivity measurements require cryptic species identification (in prep.)Google Scholar
  53. Team RC (2014) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014Google Scholar
  54. Thomas L, Palumbi SR (2017) The genomics of recovery from coral bleaching. Proceedings Biol Sci 284:20171790CrossRefGoogle Scholar
  55. Tomascik T, Van Woesik R, Mah AJ (1996) Rapid coral colonization of a recent lava flow following a volcanic eruption, Banda Islands, Indonesia. Coral Reefs 15:169–175CrossRefGoogle Scholar
  56. Wakeford M, Done TJ, Johnson CR (2008) Decadal trends in a coral community and evidence of changed disturbance regime. Coral Reefs 27:1–13CrossRefGoogle Scholar
  57. Warner PA, Oppen MJH, Willis BL (2015) Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial-genetic patterns of connectivity. Mol Ecol 24:2993–3008CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUCLALos AngelesUSA
  2. 2.Department of BiologyStanford UniversityPacific GroveUSA

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