Marine Biology

, Volume 161, Issue 2, pp 395–409 | Cite as

Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia

  • Natasha A. Hardy
  • Miles Lamare
  • Sven Uthicke
  • Kennedy Wolfe
  • Steve Doo
  • Symon Dworjanyn
  • Maria Byrne
Original Paper

Abstract

The thermal envelope of development to the larval stage of two echinoids from eastern Australia was characterized to determine whether they fill their potential latitudinal ranges as indicated by tolerance limits. The tropical sand dollar, Arachnoides placenta, a species that is not known to have shifted its range, was investigated in Townsville, northern Australia (19°20′S, 146°77′E), during its autumn spawning season (May 2012). The subtropical/temperate sea urchin, Centrostephanus rodgersii, a species that has undergone poleward range expansion, was investigated in Sydney, southern Australia (33°58′S, 151°14′E), during its winter spawning season (August 2012). The thermal tolerance of development was determined in embryos and larvae reared at twelve temperatures. For A. placenta, the ambient water temperature near Townsville and experimental control were 24 °C and treatments ranged from 14 to 37 °C. For C. rodgersii, ambient Sydney water temperature and experimental control were 17 °C, and the treatment range was 9–31 °C. A. placenta had a broader developmental thermal envelope (14 °C range 17–31 °C) than C. rodgersii (9 °C range 13–22 °C). Both species developed successfully at temperatures well below ambient, suggesting that cooler water is not a barrier to poleward migration for either species. Both species presently live near the upper thermal limits for larval development, and future ocean warming could lead to contractions of their northern range limits. This study provides insights into the factors influencing the realized and potential distribution of planktonic life stages and changes to adult distribution in response to global change.

Supplementary material

227_2013_2344_MOESM1_ESM.doc (3.2 mb)
Supplementary material 1 (DOC 3317 kb)

References

  1. Andronikov VB (1975) Heat resistance of gametes of marine invertebrates in relation to temperature conditions under which the species exist. Mar Biol 30:1–11CrossRefGoogle Scholar
  2. Baird AH, Sommer B, Madin JS (2012) Pole-ward range expansion of Acropora spp. along the east coast of Australia. Coral Reefs. doi:10.1007/s00338-012-0928-6 Google Scholar
  3. Banks SC, Piggott MP, Williamson JE, Bové U, Holbrook NJ, Beheregaray LB (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064CrossRefGoogle Scholar
  4. Banks SC, Ling SD, Johnson CR, Piggott MP, Williamson JE, Beheregaray LB (2010) Genetic structure of a recent climate change-driven range extension. Mol Ecol 19:2011–2024CrossRefGoogle Scholar
  5. Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672–675CrossRefGoogle Scholar
  6. Booth DJ, Figueira WF, Gregson MA, Brown L, Beretta G (2007) Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current. Estuar Coast Shelf Sci 72:102–114CrossRefGoogle Scholar
  7. Byrne M (2010) Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: Yu J, Henderson-Sellers A (eds) Climate alert: climate change monitoring and strategy. University of Sydney Press, Sydney, pp 142–185Google 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. Ocean Mar Biol Annu Rev 49:1–42Google Scholar
  9. Byrne M, Andrew NL (2013) Centrostephanus rodgersii. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier Science, AmsterdamGoogle Scholar
  10. Byrne M, Soars N, Ho M-A, Wong E, McElroy D, Selvakumaraswamy P, Sheppard-Brennand H, Dworjanyn SA, Davis AR (2010) Fertilisation in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification. Mar Biol 157:2061–2069CrossRefGoogle Scholar
  11. Byrne M, Selvakumaraswamy P, Ho M-A, Nguyen HD (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep-Sea Res 58:712–719CrossRefGoogle Scholar
  12. Chen C-P, Chen B-Y (1992) Effects of high temperature on larval development and metamorphosis of Arachnoides placenta (Echinodermata: Echinoidea). Mar Biol 112:445–449CrossRefGoogle Scholar
  13. Condie SA, Dunn JR (2006) Seasonal characteristics of the surface mixed layer in the Australasian region: implications for primary production regimes and biogeography. Mar Freshw Res 57:569–590CrossRefGoogle Scholar
  14. Doo SS, Dworjanyn SA, Foo SA, Soars NA, Byrne M (2012) Impacts of ocean acidification on development of the meroplanktonic larval stage of the sea urchin Centrostephanus rodgersii. ICES J Mar Sci 69:460–464CrossRefGoogle Scholar
  15. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefGoogle Scholar
  16. Figueira WF, Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive over winter in temperate waters. Glob Change Biol 16:506–516CrossRefGoogle Scholar
  17. Foo SA, Dworjanyn SA, Poore AGB, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS ONE 7:e42497CrossRefGoogle Scholar
  18. Fujisawa H (1989) Differences in temperature dependence of early development of sea urchins with different growing seasons. Biol Bull 176:96–102CrossRefGoogle Scholar
  19. Fujisawa H (1995) Variation in embryonic temperature sensitivity among groups of the sea urchin, Hemicentrotus pulcherrimus, which differ in their habitats. Zool Sci 12:583–589CrossRefGoogle Scholar
  20. Gonzalez-Bernat MJ, Lamare M, Uthicke S, Byrne M (2013) Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH. Mar Biol 160:1927–1941. doi:10.1007/s00227-012-2034-2 CrossRefGoogle Scholar
  21. Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282CrossRefGoogle Scholar
  22. Hadfield MG, Strathmann MF (1996) Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanol Acta 19:323–324Google Scholar
  23. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci 104:1745–1750CrossRefGoogle Scholar
  24. Hart MW, Scheibling RE (1988) Heat waves, baby booms and the destruction of kelp beds by sea urchins. Mar Biol 99:167–176CrossRefGoogle Scholar
  25. Hart MW, Strathmann RR (1994) Functional consequences of phenotypic plasticity in echinoid larvae. Biol Bull 186:291–299CrossRefGoogle Scholar
  26. Haycock LJ (2004) The reproduction and recruitment of the sand dollar Arachnoides placenta (L.) (Echinoidea: Echinodermata) from differing habitats on the North Queensland coast. MS Research Thesis, James Cook University, QueenslandGoogle Scholar
  27. Higgins FA, Bates AE, Lamare MD (2012) Heat tolerance, behavioural temperature selection and temperature-dependent respiration in larval Octopus huttoni. J Therm Biol 37:83–88CrossRefGoogle Scholar
  28. Hobday AJ, Lough JM (2011) Observed climate change in Australian marine and freshwater environments. Mar Freshw Res 62:984–999CrossRefGoogle Scholar
  29. Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability, and the development of marine invertebrate larvae. Am Zool 14:415–425Google Scholar
  30. International Panel on Climate Change (IPCC) (2007) Climate change 2007: the fourth assessment report of the International Panel on Climate Change (IPCC). Cambridge University Press, CambridgeCrossRefGoogle Scholar
  31. Johnson LG, Babcock RC (1994) Temperature and the larval ecology of the Crown-of-thorns starfish, Acanthaster planci. Biol Bull 187:304–308CrossRefGoogle Scholar
  32. Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F, Hill KL, Holbrook NJ, Hosie GW, Last PR, Ling SD, Melbourne-Thomas J, Miller K, Pecl GT, Richardson AJ, Ridgway KR, Rintoul SR, Ritz DA, Ross DJ, Sanderson JC, Shepherd SA, Slotwinski A, Swadling KA, Taw N (2012) Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Biol Ecol 400:17–32CrossRefGoogle Scholar
  33. Jones SJ, Mieszkowska N, Wethey DS (2009) Linking thermal tolerances and biogeography: Mytilus edulis (L.) at its southern limit on the east coast of the United States. Biol Bull 217:73–85Google Scholar
  34. Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Change Biol 14:907–915CrossRefGoogle Scholar
  35. Ling SD, Johnson CR, Ridgway K, Hobday AJ, Haddon M (2009) Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob Change Biol 15:719–731CrossRefGoogle Scholar
  36. McEdward LR (1985) Effects of temperature on the body form, growth, electron transport system activity, and development rate of an echinopluteus. J Exp Mar Biol Ecol 93:169–181CrossRefGoogle Scholar
  37. Miskelly A (2002) Sea urchins of Australia and the Indo-Pacific. Capricornia Publications, SydneyGoogle Scholar
  38. Morley SA, Martin SM, Day RW, Ericson J, Lai C-H, Lamare M, Tan K-S, Thorne MAS, Peck LS (2012) Thermal reaction norms and the scale of temperature variation: latitudinal vulnerability of intertidal nacellid limpets to climate change. PlosOne 7:e52818CrossRefGoogle Scholar
  39. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution and conservation. Proc Natl Acad Sci 104:1266–1271CrossRefGoogle Scholar
  40. Palmer AR (1994) Temperature sensitivity, rate of development, and time to maturity: geographic variation in laboratory reared Nucella and a cross-phyletic overview. In: Wilson WH Jr, Stricker SA, Shin GL (eds) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 177–194Google Scholar
  41. Pearse JS, Pearse VB, Davis KK (1986) Photoperiodic regulation of gametogenesis and growth in the sea urchin Strongylocentrotus purpuratus. J Exp Zool 237:107–118CrossRefGoogle Scholar
  42. Pechenik JA (1987) Environmental influences on larval survival and development. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates. Academic Press, New York, pp 551–608Google Scholar
  43. Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Int Comp Biol 46:323–333CrossRefGoogle Scholar
  44. Pecorino D, Lamare MD, Barker MF, Byrne M (2013) Does embryonic and larval thermal tolerance control the distribution of the sea urchin Centrostephanus rodgersii (Diadematidae) in New Zealand? J Exp Mar Biol Ecol 445:120–128CrossRefGoogle Scholar
  45. Poloczanska ES, Babcock RC, Butler A, Hobday A, Hoegh-Guldberg O, Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007) Climate change and Australian marine life. Oceanogr Mar Biol Annu Rev 45:407–478Google Scholar
  46. Pörtner H-O, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefGoogle Scholar
  47. Pörtner H-O, Peck L, Somero GN (2007) Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view. Philos Trans R Soc B 362:2233–2258CrossRefGoogle Scholar
  48. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  49. Rahman S, Tsuchiya M, Uehara T (2009) Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia 64:768–775CrossRefGoogle Scholar
  50. Rassoulzadegan F, Fenaux L (1979) Grazing of echinoderm larvae (Paracentrotus lividus and Arbacia lixula) on naturally occurring particulate matter. J Plankton Res 1:215–223CrossRefGoogle Scholar
  51. Reitzel AM, Miles CM, Heyland A, Cowart JD, McEdward LR (2005) The contribution of the facultative feeding period to echinoid larval development and size at metamorphosis: a comparative approach. J Exp Mar Biol Ecol 317:189–201CrossRefGoogle Scholar
  52. Ridgway KR (2007) Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett 34:L13613CrossRefGoogle Scholar
  53. Rupp JH (1973) Effects of temperature on fertilization and early cleavage of some tropical echinoderms, with emphasis on Echinometra mathaei. Mar Biol 23:183–189CrossRefGoogle Scholar
  54. Sewell MA, Young CM (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. J Exp Mar Biol Ecol 236:291–305CrossRefGoogle Scholar
  55. Short AD (1993) Beaches of the New South Wales Coast: a guide to their nature, characteristics, surf and safety. Australian Beach Safety and Management Program, NSWGoogle Scholar
  56. Soars NA, Prowse TAA, Byrne M (2009) Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus transversus’ type vs. typical echinoplutei. Mar Ecol Prog Ser 383:113–125CrossRefGoogle Scholar
  57. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920CrossRefGoogle Scholar
  58. Storch D, Fernández M, Navarrete SA, Pörtner H-O (2011) Thermal tolerance of larval stages of the Chilean kelp crap Taliepus dentatus. Mar Ecol Prog Ser 429:157–167CrossRefGoogle Scholar
  59. Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830CrossRefGoogle Scholar
  60. Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686–690Google Scholar
  61. Swanson RL, Byrne M, Prowse TAA, Mos B, Dworjanyn SA, Steinberg PD (2012) Dissolved histamine: a potential habitat marker promoting settlement and metamorphosis in sea urchins larvae. Mar Biol 159:915–925CrossRefGoogle Scholar
  62. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  63. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  64. Wernberg T, Russel 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
  65. Wolfe KDL, Dworjanyn SA, Byrne M (2013) Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin, (Heliocidaris erythrogramma). Glob Change Biol 19:2608–2707Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Natasha A. Hardy
    • 1
  • Miles Lamare
    • 2
  • Sven Uthicke
    • 3
  • Kennedy Wolfe
    • 1
    • 4
  • Steve Doo
    • 1
    • 4
  • Symon Dworjanyn
    • 5
  • Maria Byrne
    • 1
    • 4
  1. 1.School of Medical SciencesUniversity of SydneySydneyAustralia
  2. 2.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  3. 3.Australian Institute of Marine ScienceTownsvilleAustralia
  4. 4.School of Biological SciencesUniversity of SydneySydneyAustralia
  5. 5.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia

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