Coral Reefs

, Volume 36, Issue 1, pp 325–338 | Cite as

Paternal identity influences response of Acanthaster planci embryos to ocean acidification and warming

  • Kate M. Sparks
  • Shawna A. Foo
  • Sven Uthicke
  • Maria Byrne
  • Miles Lamare


The crown-of-thorns sea star Acanthaster planci is a key predator of corals and has had a major influence on the decrease in coral cover across the Indo-Pacific. To understand how this species may adapt to ocean warming and acidification, this study used a quantitative genetic approach to examine the response in offspring of 24 half-sib A. planci families raised in fully crossed treatment combinations of temperature (27, 29 and 31 °C) and pCO2 (450 and 900 ppm) to the gastrulation stage (26 h post-fertilisation). Interactions between genotype and environment were tested using a permutational multivariate ANOVA and restricted error maximum likelihood calculations of variance. High temperature (31 °C) significantly reduced normal (symmetrical, intact) development by ~15% at the 16-cell stage. Increased temperature (from 29 to 31 °C) reduced normal gastrulation from ~65 to ~30%. The extent to which each genotype was affected depended on sire identity, which explained 15% of variation. pCO2 did not significantly influence development at gastrulation. To explore the importance of individual mating pairs, response ratios were calculated for offspring of each family across all treatments. Response ratios demonstrated that the majority of genotypes experienced the highest percentage of normal development to gastrulation in the control treatment, and that family (sire × dam) is important in determining the response to ocean warming and acidification. A positive genetic correlation (overall r*G = 0.76) from sire × environment interactions, however, indicated that individuals which develop ‘better’ at both high temperature and high pCO2 may cope better with near-future predicted warm and acidified conditions for eastern Australia.


Acanthaster planci Ocean warming Ocean acidification Adaptation Crown-of-thorns sea star Great Barrier Reef 



Research was supported by the Australian Institute of Marine Science and carried out in the National Sea Simulator (SeaSim). Water chemistry analysis was carried out by Stephen Boyle at AIMS. The authors would like to thank SeaSim staff especially Andreas Severati for engineering and technical support in the SeaSim unit, and Michelle Liddy for assistance with data collection. The authors would like to acknowledge funding from a University of Sydney Scholarship (S. Foo) and from the University of Otago (K. Sparks and M. Lamare). This is Sydney Institute of Marine Science contribution number 187.

Supplementary material

338_2016_1505_MOESM1_ESM.docx (802 kb)
Supplementary material 1 (DOCX 803 kb)


  1. Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshell PA, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Chang Biol 17:1798–1808CrossRefPubMedCentralGoogle Scholar
  2. Appelhans YS, Thomsen J, Opitz S, Pansch C, Melzner F, Wahl J (2014) Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential. Mar Ecol Prog Ser 509:227–239CrossRefGoogle Scholar
  3. Babcock RC (1990) Spawning behaviour of Acanthaster planci. Coral Reefs 9:124–127CrossRefGoogle Scholar
  4. Babcock RC, Mundy CN (1992) Reproductive biology, spawning and field fertilization rates of Acanthaster planci. Aust J Mar Freshw Res 43:525–533CrossRefGoogle Scholar
  5. Bellwood D, Hughes T, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  6. Brodie J, Fabricius K, De’ath G, Okaji K (2005) Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence. Mar Pollut Bull 51:266–278CrossRefPubMedGoogle Scholar
  7. Busby PE, Newcombe G, Dirzo R, Whitman TG (2014) Differentiating genetic and environmental drivers of plant–pathogen community interactions. J Ecol 102:1300–1309CrossRefGoogle Scholar
  8. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Ann Rev Oceanog Mar Biol 49:1–42Google Scholar
  9. Byrne M, Gonzalez-Bernat M, Doo S, Foo S, Soars N, Lamare M (2013) Effects of ocean warming and acidification on embryos and non-calcifying larvae of the invasive sea star Patiriella regularis. Mar Ecol Prog Ser 473:235–246CrossRefGoogle Scholar
  10. Byrne M, Prowse TAA, Sewell MA, Dworjanyn S, Williamson JE, Vaitilingon D (2008) Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla. Mar Biol 155:473–482CrossRefGoogle Scholar
  11. Byrne M, Villinski J, Popodi E, Cisternas P, Raff R (1999) Maternal factors and the evolution of developmental mode: evolution of oogenesis in Heliocidaris erythrogramma. Dev Genes Evol 209:275–283CrossRefPubMedGoogle Scholar
  12. Byrne M (2010) Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: You Y, Henderson-Sellers A (eds) Climate alert: climate change monitoring and strategy. Sydney University Press, Sydney, Australia, pp 142–185Google Scholar
  13. Bürger R, Lynch M (1997) Adaptation and extinction in changing environments. In: Bijlsma R, Loeschcke V (eds) Environmental stress, adaptation and evolution. Springer, Basel, pp 209–239CrossRefGoogle Scholar
  14. Clark KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  15. Clark JS, Poore AGB, Ralph PJ, Doblin MA (2013) Potential for adaptation in response to thermal stress in an intertidal macroalga. J Phycol 49:630–639CrossRefPubMedGoogle Scholar
  16. Crain WR, Bushman FD (1983) Transcripts of paternal and maternal actin gene alleles are present in interspecific sea urchin embryo hybrids. Dev Biol 100:190–196CrossRefPubMedGoogle Scholar
  17. Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94:2575–2582CrossRefPubMedGoogle Scholar
  18. Dahlhoff EP, Fearnley SL, Bruce DA, Gibbs AG, Stoneking R, McMillan DM, Smiley JT, Rank NE (2008) Effects of temperature on physiology and reproductive success of a montane leaf beetle: implications for persistence of native populations enduring climate change. Physiol Biochem Zool 81:718–732CrossRefPubMedGoogle Scholar
  19. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci U S A 109:17995–17999CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res A 34:1733–1743CrossRefGoogle Scholar
  21. Dickson AG, Sabine CL, Christian JR (eds) (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3. North Pacific Marine Science Organization, Sidney, British Columbia, p 191Google Scholar
  22. Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416CrossRefGoogle Scholar
  23. Eisen EJ, Saxton AM (1983) Genotype by environment interactions and genetic correlations involving two environmental factors. Theor Appl Genet 67:75–86CrossRefPubMedGoogle Scholar
  24. Emlet RB, McEdward LR, Strathmann R (1987) Echinoderm larval ecology as viewed from the egg. Echinoderm Studies 2:55–136Google Scholar
  25. Fabricius KE, 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
  26. Fabricius KE, Okaji K, De’ath G (2010) Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29:593–605CrossRefGoogle Scholar
  27. Falkner I, Byrne M, Sewell MA (2006) Maternal provisioning in Ophionereis fasciata and O.schayeri: brittle stars with contrasting modes of development. Biol Bull 211:204–207CrossRefPubMedGoogle Scholar
  28. Foo SA, Byrne M (2016) Acclimatization and adaptive capacity of marine species in a changing ocean. Adv Mar Biol. doi: 10.1016/bs.amb.2016.06.001 PubMedGoogle Scholar
  29. Foo SA, Dworjanyn SA, Khatkar MS, Poore AGB, Byrne M (2014) Increased temperature, but not acidification, enhances fertilisation and development in a tropical urchin: potential for adaptation to a tropicalised eastern Australia. Evol Appl 7:1226–1237CrossRefPubMedPubMedCentralGoogle Scholar
  30. Foo SA, Dworjanyn SA, Poore AGB, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and acidification: performance of early embryos. PLoS One 7:e42497CrossRefPubMedPubMedCentralGoogle Scholar
  31. Garcia E, Clemente S, Hernandez JC (2015) Ocean warming ameliorates the negative effects of ocean acidification on Paracentrotus lividus larval development and settlement. Mar Environ Res 110:61–68CrossRefPubMedGoogle Scholar
  32. Gianguzza P, Visconti G, Gianguzza F, Vizzini S, Sara G, Dupont S (2014) Temperature modulates the response of the thermophilous sea urchin Arbacia lixula early life stages to CO2-driven ocean acidification. Mar Environ Res 93:70–77CrossRefPubMedGoogle Scholar
  33. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178CrossRefPubMedGoogle Scholar
  34. Gonzalez-Bernat M, Lamare M, Barker M (2013) Effects of reduced seawater pH on fertilisation, embryogenesis and larval development in the Antarctic seastar Odontaster validus. Polar Biol 36:235–247CrossRefGoogle Scholar
  35. Gooding RA, Harley CG, Tang E (2009) Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proc Natl Acad Sci U S A 106:9316–9321CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci U S A 104:1745–1750CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hardy NA, Byrne M (2014) Early development of congeneric sea urchins (Heliocidaris) with contrasting life history modes in a warming and high CO2 ocean. Mar Environ Res 102:78–87CrossRefPubMedGoogle Scholar
  38. Harris JL (2015) Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Mar Ecol Prog Ser 532:41–57CrossRefGoogle Scholar
  39. Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptaion action. Rev Fish Biol Fish 24:415–425CrossRefGoogle Scholar
  40. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  41. Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability and the development of marine invertebrate larvae. Am Zool 35:415–425CrossRefGoogle Scholar
  42. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485CrossRefPubMedGoogle Scholar
  43. Hoffmann AA, Shirriffs J, Scott M (2005) Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct Ecol 19:222–227CrossRefGoogle Scholar
  44. IPCC (Intergovernmental Panel on Climate Change) (2007) Climate change 2013: the 4th assessment report of the IPCC. Cambridge University Press, Cambridge, UKGoogle Scholar
  45. Johnson LG, Babcock RC (1994) Temperature and the larval ecology of the crown-of-thorns starfish, Acanthaster planci. Biol Bull 187:304–308CrossRefGoogle Scholar
  46. Kamya PZ, Dworjanyn SA, Hardy N, Moss B, Uthicke S, Byrne M (2014) Larvae of the coral eating crown-of-thorns starfish, Acanthaster planci in a warmer-high CO2 ocean. Glob Chang Biol 20:3365–3376CrossRefPubMedGoogle Scholar
  47. Kelly MW, Padilla-Gamino JL, Hofmann GE (2013) Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Glob Chang Biol 19:2536–2546CrossRefPubMedGoogle Scholar
  48. Lamare M, Pecorino D, Hardy N, Liddy M, Byrne M, Uthicke S (2014) The thermal tolerance of crown-of-thorns (Acanthaster planci) embryos and bipinnaria larvae: implications for spatial and temporal variation in adult populations. Coral Reefs 33:207–219CrossRefGoogle Scholar
  49. Lamit LJ, Lau MK, Næsborg RR, Wojtowicz T, Whitman TG, Gehring CA (2015) Genotype variation in bark texture drives lichen community assembly across multiple environments. Ecology 96:960–971CrossRefPubMedGoogle Scholar
  50. Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446CrossRefPubMedGoogle Scholar
  51. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Centre, U.S. Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  52. Lough JM, Hobday AJ (2011) Observed climate change in Australian marine and freshwater environments. Mar Freshw Res 62:984–999CrossRefGoogle Scholar
  53. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  54. Malvezzi AJ, Murray CS, Feldheim KA, DiBattista JD, Garant D, Gobler CJ, Chapman DD, Baumann H (2015) A quantitative genetic approach to assess the evolutionary potential of a coastal marine fish to ocean acidification. Evol Appl 8:352–362CrossRefPubMedPubMedCentralGoogle Scholar
  55. Marshall DJ, Heppell SS, Munch SB, Warner RR (2010) The relationship between maternal phenotypes and offspring quality: do older mothers really produce the best offspring? Ecology 91:2862–2873CrossRefPubMedGoogle Scholar
  56. Mehrbach C, Culbertson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation of carbonic acid in seawater at atmoshperic pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  57. Merilä J, Hendry AP (2014) Climate change, adaptation and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14CrossRefPubMedPubMedCentralGoogle Scholar
  58. Moran PJ, Bradbury RH, Reichelt RE (1988) Distribution of recent outbreaks of the crown-of-thorns starfish (Acanthaster planci L.) along the Great Barrier Reef: 1985–1986. Coral Reefs 7:125–137CrossRefGoogle Scholar
  59. Moran PJ, De’ath G (1992) Estimates of the abundance of the crown-of-thorns starfish Acanthaster planci in outbreaking and non-outbreaking populations on reefs within the Great Barrier Reef. Mar Biol 113:509–515CrossRefGoogle Scholar
  60. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16:1488–1500CrossRefPubMedGoogle Scholar
  61. Nguyen H, Byrne M (2014) Early benthic juvenile Parvulastra exigua (Asteroidea) are tolerant to extreme acidification and warming in its intertidal habitat. J Exp Mar Bio Ecol 453:36–42CrossRefGoogle Scholar
  62. Nguyen H, Doo SS, Soars NA, Byrne M (2012) Noncalcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star Meridiastra calcar. Glob Chang Biol 18:2466–2476CrossRefGoogle Scholar
  63. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686CrossRefPubMedGoogle Scholar
  64. Patiño S, Keever CC, Sunday JM, Popovic I, Byrne M, Hart MW (2016) Sperm bindin divergence under sexual selection and concerted evolution in sea stars. Mol Biol Evol. doi: 10.1093/molbev/msw081 PubMedGoogle Scholar
  65. Pearson RG, Endean R (1969) A preliminary study of the coral predator Acanthaster planci (L.) (Asteroidea) on the Great Barrier Reef. Fish Notes 3:27–55Google Scholar
  66. Pespeni MH, Sanford E, Gaylord B, Hill TM, Hosfelt JD, Jaria HK, LaVigne M, Lenz EA, Russell AD, Young MK, Palumbi SR (2013) Evolutionary change during experimental ocean acidification. Proc Natl Acad Sci U S A 110:6937–6942CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pratchett MS (2005) Dynamics of an outbreak population of Acanthaster planci at Lizard Island, northern Great Barrier Reef 1995–1999. Coral Reefs 24:453–462CrossRefGoogle Scholar
  68. Pratchett MS, Caballes CF, Pivera-Posada JA, Sweatman HPA (2014) Limits to understanding and managing outbreaks of crown-of-thorns starfish (Acanthaster spp.). Oceanogr Mar Biol Annu Rev 52:133–200CrossRefGoogle Scholar
  69. Prowse TAA, Sewell MA, Byrne M (2008) Fuels for development: evolution of maternal provisioning in asterinid sea stars. Mar Biol 153:337–349CrossRefGoogle Scholar
  70. Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine invertebrates and larvae. Glob Chang Biol 21:2122–2140CrossRefPubMedGoogle Scholar
  71. Roche RC, Pratchett MS, Carr P, Turner JR, Wagner D, Head C, Sheppard CRC (2015) Localized outbreaks of Acanthaster planci at an isolated and unpopulated reef atoll in the Chagos Archipelago. Mar Biol 162:1695–1704CrossRefGoogle Scholar
  72. Searle SR, Casella G, McCulloch CE (1992) Variance components. John Wiley and Sons, New York, USACrossRefGoogle Scholar
  73. Shaw EC, McNeil BI (2014) Seasonal variability in carbonate chemistry and air–sea CO2 fluxes in the southern Great Barrier Reef. Mar Chem 158:49–58CrossRefGoogle Scholar
  74. Sunday JM, Calosi P, Dupont S, Munday PS, Stillman JS, Reusch TB (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125CrossRefPubMedGoogle Scholar
  75. Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quanitfying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881CrossRefPubMedPubMedCentralGoogle Scholar
  76. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042CrossRefPubMedGoogle Scholar
  77. Terlizzi A, Anderson MJ, Fraschetti S, Benedetti-Cecchi L (2007) Scales of spatial variation on Mediterranean subtidal sessile assemblages at different depths. Mar Ecol Prog Ser 332:25–39CrossRefGoogle Scholar
  78. Uthicke S, Logan M, Liddy M, Francis D, Hardy N, Lamare MD (2015) Climate change as an unexpected co-factor promoting coral eating seastar (Acanthaster planci) outbreaks. Sci Rep 5:8402CrossRefPubMedPubMedCentralGoogle Scholar
  79. Uthicke S, Pecorino D, Allbright R, Negri AP, Cantin N, Liddy M, Dworjanyn S, Kamya P, Byrne M, Lamare M (2013) Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci. PLoS One 8:e82938CrossRefPubMedPubMedCentralGoogle Scholar
  80. Uthicke S, Schaffelke B, Byrne M (2009) A boom-bust phylum? Ecological and evolutionary consequences of density variations in Echinoderms. Ecol Monogr 79:3–24CrossRefGoogle Scholar
  81. Villinski JT, Villinski JC, Byrne MA, Raff RA (2002) Convergent maternal provisioning and life history evolution in Echinoderms. Evolution 56:1764–1775CrossRefPubMedGoogle Scholar
  82. Wolfe K, Graba-Landry A, Dworjanyn SA, Byrne M (2015a) Larval starvation to satiation: influence of nutrient regime on the success of Acanthaster planci. PLoS One 10:e0122010CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wolfe K, Graba-Landry A, Dworjanyn SA, Byrne M (2015b) Larval phenotypic plasticity in the boom-and-bust Crown-of-Thorns starfish Acanthaster planci. Mar Ecol Prog Ser 539:179–189CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Kate M. Sparks
    • 1
  • Shawna A. Foo
    • 2
  • Sven Uthicke
    • 3
  • Maria Byrne
    • 4
  • Miles Lamare
    • 1
  1. 1.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  2. 2.School of Medical SciencesUniversity of SydneySydneyAustralia
  3. 3.Australian Institute of Marine ScienceTownsvilleAustralia
  4. 4.Schools of Medical and Biological SciencesUniversity of SydneySydneyAustralia

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