Marine Biology

, Volume 157, Issue 9, pp 2061–2069

Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification

  • Maria Byrne
  • Natalie A. Soars
  • Melanie A. Ho
  • Eunice Wong
  • David McElroy
  • Paulina Selvakumaraswamy
  • Symon A. Dworjanyn
  • Andrew R. Davis
Original Paper

Abstract

Climate change driven ocean acidification and hypercapnia may have a negative impact on fertilization in marine organisms because of the narcotic effect these stressors exert on sperm. In contrast, warmer, less viscous water may have a positive influence on sperm swimming speed and so ocean warming may enhance fertilization. To address questions on future vulnerabilities we examined the interactive effects of near-future ocean warming and ocean acidification/hypercapnia on fertilization in intertidal and shallow subtidal echinoids (Heliocidaris erythrogramma, H. tuberculata, Tripneustes gratilla, Centrostephanus rodgersii), an asteroid (Patiriella regularis) and an abalone (Haliotis coccoradiata). Batches of eggs from multiple females were fertilized by sperm from multiple males in all combinations of three temperature and three \( {\text{pH}}/P_{{{\text{CO}}_{2} }} \) treatments. Experiments were placed in the setting of projected near-future conditions for southeast Australia, an ocean change hot spot. There was no significant effect of warming and acidification on the percentage of fertilization. These results indicate that fertilization in these species is robust to temperature and \( {\text{pH}}/P_{{{\text{CO}}_{2} }} \) fluctuation. This may reflect adaptation to the marked fluctuation in temperature and pH that characterises their shallow water coastal habitats. Efforts to identify potential impacts of ocean change to the life histories of coastal marine invertebrates are best to focus on more vulnerable embryonic and larval stages because of their long time in the water column where seawater chemistry and temperature have a major impact on development.

References

  1. Allen JD, Pechenik JA (2010) Understanding the effects of low salinity on fertilization success and early development in the sand dollar Echinarachnius parma. Biol Bull 218:189–199PubMedGoogle Scholar
  2. Andrew NL, Byrne M (2007) Centrostephanus. In: Lawrence JM (ed) The biology and ecology of edible urchins. Elsevier Science, Amsterdam, pp 191–204Google Scholar
  3. ASTM (2004) Standard guide for conducting static acute toxicity tests with echinoid embryos. E 1563–98. American Society for Testing and Materials, PhiladelphiaGoogle Scholar
  4. Baker MC, Tyler PA (2001) Fertilization success in the commercial gastropod Haliotis tuberculata. Mar Ecol Prog Ser 211:205–213CrossRefGoogle Scholar
  5. Bay S, Burgess R, Nacci D (1993) Status and applications of echinoid (Phylum Echinodermata) toxicity test methods. In: Wayne G, Hughes JS, Lewis MA (eds) Environmental Toxicology and Risk Assessment, ASTM STP 1179. American Society of Testing and Materials, Philadelphia, pp 281–302CrossRefGoogle Scholar
  6. Bingham BL, Bacigalupi M, Johnson LG (1997) Temperature adaptations of embryos from intertidal and subtidal sand dollars (Dendraster excentricus, Eschscholtz). Northw Sci 71:108–114Google Scholar
  7. Björk M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast. Mar Ecol Prog Ser 284:109–116CrossRefGoogle Scholar
  8. Bolton TF, Havenhand JN (1996) Chemical mediation of sperm activity and longevity in the solitary ascidians Ciona intestinalis and Ascidiella aspersa. Biol Bull 190:329–335CrossRefGoogle Scholar
  9. Bookbinder LH, Shick JM (1986) Anaerobic and aerobic energy metabolism in ovaries of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 93:103–110CrossRefGoogle Scholar
  10. Brokaw CJ (1990) The sea urchin spermatozoon. BioEssays 12:449–452CrossRefPubMedGoogle Scholar
  11. Byrne M (2010) Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata. In: Yu Y, Henderson-Sellers A (eds) Climate alert: climate change monitoring and strategy. University of Sydney Press, Sydney, pp 142–185Google Scholar
  12. Byrne RH, Kump LR, Cantrell KJ (1988) The influence of temperature and pH on trace metal speciation in seawater. Mar Chem 25:163–181CrossRefGoogle Scholar
  13. Byrne M, Andrew NL, Worthington DG, Brett PA (1998) The influence of latitude and habitat on reproduction in the sea urchin Centrostephanus rodgersii in New South Wales, Australia. Mar Biol 132:305–318CrossRefGoogle Scholar
  14. Byrne M, Oakes DJ, Pollak JK, Laginestra E (2008) Toxicity of landfill leachate to sea urchin development with a focus on ammonia. Cell Biol Toxicol 24:503–512CrossRefPubMedGoogle Scholar
  15. Byrne M, Ho M, Selvakumaraswamy P, Nguyen HD, Dworjanyn SA, Davis AR (2009) Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc R Soc B 276:1883–1935CrossRefPubMedGoogle Scholar
  16. Byrne M, Soars N, Selvakumaraswamy P, Dworjanyn SA, Davis AR (2010a) Sea urchin fertilization in a warm, acidified ocean and high P CO2 ocean across a range of sperm densities. Mar Environ Res 69:234–239CrossRefPubMedGoogle Scholar
  17. Byrne M, Selvakumaraswamy P, Ho MA, Nguyen HD (2010b) Sea urchin development in a global change hot spot, potential for southerly migration of thermotolerant propagules. Deep Sea Res II (in press)Google Scholar
  18. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  19. Carr RS, Biedenbach JM, Nipper M (2006) Influence of potentially confounding factors on sea urchin porewater toxicity tests. Arch Environ Contam Toxicol 51:573–579CrossRefPubMedGoogle Scholar
  20. Cherr GN, Shoffner-McGee J, Shenker JM (1990) Methods for assessing fertilization and embryonic/larval development in toxicity tests using the California mussel (Mytilus californianus). Environ Toxicol Chem 9:1137–1145Google Scholar
  21. Chia FS, Bickell LR (1983) Echinodermata. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 2. Wiley, New York, pp 545–620Google Scholar
  22. Clark D, Lamare M, Barker M (2009) Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among tropical, temperate, and a polar species. Mar Biol 156:1125–1137CrossRefGoogle Scholar
  23. Clotteau G, Dubé F (1993) Optimization of fertilization parameters for rearing surf clams (Spisula solidissima). Aquaculture 114:339–353CrossRefGoogle Scholar
  24. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315CrossRefPubMedGoogle Scholar
  25. Darszon A, Guerrero A, Galindo BE, Nishigaki T, Wood CD (2008) Sperm-activating peptides in the regulation of ion fluxes, signal transduction and motility. Int J Dev Biol 52:595–606CrossRefPubMedGoogle Scholar
  26. Desrosiers RR, Désilets J, Dubé F (1996) Early developmental events following fertilization in the giant scallop Placopecten magellanicus. Can J Fish Aquat Sci 53:1382–1392CrossRefGoogle Scholar
  27. Dinnel PA, Link JM, Stober QJ (1987) Improved methodology for a sea-urchin sperm cell bioassay for marine waters. Arch Environ Contam Toxicol 16:23–32CrossRefPubMedGoogle Scholar
  28. Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294CrossRefGoogle Scholar
  29. Dupont S, Ortega-Martínez O, Thorndyke MC (2010) Impact of near future ocean acidification on echinoderms. Ecotoxicology 19:440–462CrossRefGoogle Scholar
  30. Edgar GJ (2000) Australian marine life the plants and animals of temperate waters. Reed New Holland, Sydney, p 544Google Scholar
  31. Evans KP, Marshall DJ (2005) Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106–112PubMedGoogle Scholar
  32. Evans JP, García-González F, Marshall DJ (2007) Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61:2832–2838CrossRefPubMedGoogle Scholar
  33. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. J Mar Sci 65:414–432Google Scholar
  34. Greenwood PJ, Bennett T (1981) Some effects of temperature-salinity combinations on the early development of the sea urchin Parachinus angulosus (Leske). Fertilization. J Exp Mar Biol Ecol 51:119–131CrossRefGoogle Scholar
  35. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Nat Acad Sci USA 104:1745–1750CrossRefPubMedGoogle Scholar
  36. Havenhand JN, Schlegel P (2009) Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosci Discuss 6:4573–4586CrossRefGoogle Scholar
  37. Havenhand JN, Butler FR, Thorndyke MC, Williamson JE (2008) Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr Biol 18:651–652CrossRefGoogle Scholar
  38. Hendriks IE, Duarte CM, Álvarez A (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Est Coast Shelf Sci 86:157–164CrossRefGoogle Scholar
  39. Hoenig JM, Heisey DM (2001) The abuse of power: the pervasive fallacy of power calculations for data analysis. Am Stat 55:19–24CrossRefGoogle Scholar
  40. Holland LZ, Gould-Somero M, Paul M (1984) Fertilization acid release in Urechis eggs. I. The nature of the acid and the dependence of acid release and egg activation on external pH. Dev Biol 103:337–342CrossRefPubMedGoogle Scholar
  41. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: the fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University press, Cambridge UKGoogle Scholar
  42. Johnson CH, Clapper DL, Winkler MM, Lee HC, Epel D (1983) A volatile inhibitor immobilizes sea urchin sperm in semen by depressing the intracellular pH. Dev Biol 98:493–501CrossRefPubMedGoogle Scholar
  43. Keesing JK (2007) Ecology of Heliocidaris erythrogramma. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier Science, Amsterdam, pp 339–351Google Scholar
  44. Knutzen J (1981) Effects of decreased pH on marine organisms. Mar Pollut Bull 12:25–29CrossRefGoogle Scholar
  45. Kupriyanova EK, Havenhand JN (2005) Effects of temperature on sperm swimming behaviour, respiration and fertilization success in the serpulid polychaete, Galeolaria casepitosa (Annelida: Serpulidae). Invertebr Reprod Dev 48:7–17Google Scholar
  46. Kurihara H (2008) Effects of CO2-driven ocean acidification on the early development stages of invertebrates. Mar Ecol Prog Ser 373:275–284CrossRefGoogle Scholar
  47. Kurihara H, Shirayama Y (2004) Effects of increased atmospheric CO2 on sea urchin early development. Mar Ecol Prog Ser 274:161–169CrossRefGoogle Scholar
  48. Laegdsgaard P, Byrne M, Anderson DT (1991) Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Mar Biol 110:359–374CrossRefGoogle Scholar
  49. Lee CH, Ryu TK, Choi JW (2004) Effects of water temperature on embryonic development in the northern Pacific asteroid, Asterias amurensis, from the southern coast of Korea. Invertebr Reprod Dev 45:109–116Google Scholar
  50. Lenth RV (2001) Some practical guidelines for effective sample size determination. Am Stat Assoc 55:187–193Google Scholar
  51. Lera S, Maccia S, Pellegrini D (2006) Standardizing the methodology of the sperm cell test with Paracentrotus lividus. Environ Monitoring Assess 122:101–109CrossRefGoogle Scholar
  52. Levitan DR, Ferrell DL (2006) Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312:269–2667CrossRefGoogle Scholar
  53. Levitan DR, Sewell MA, Chia F–S (1991) Kinetics of fertilization in the sea urchin Strongylocentrotus franciscanus: interaction of gamete dilution, age, and contact time. Biol Bull 181:371–378CrossRefGoogle Scholar
  54. Levitan DR, terHorst CP, Fogarty ND (2007) The risk of polyspermy in three congeneric sea urchins and its implications for gametic incompatability and reproductive isolation. Evolution 61:2009–2016CrossRefGoogle Scholar
  55. 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. Global Change Biol 15:719–731CrossRefGoogle Scholar
  56. Marshall DJ, Evans JP (2007) Context-dependent benefits of polyandry in a marine hermpahrodite. Biol Lett 3:685–688CrossRefPubMedGoogle Scholar
  57. McLusky DS, Bryant V, Campbell R (1986) The effects of temperature and salinity on the toxicity of heavy metals to marine and estuarine invertebrates. Oceanogr Mar Biol Ann Rev 24:481–520Google Scholar
  58. Mead KS, Epel D (1995) Beakers versus breakers: how fertilization in the laboratory differs from fertilization in nature. Zygote 3:95–99CrossRefPubMedGoogle Scholar
  59. Mita M, Hino A, Yasumasu I (1984) Effect of temperature on interaction between eggs and spermatozoa of sea urchin. Biol Bull 166:68–77CrossRefGoogle Scholar
  60. Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2010) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107CrossRefPubMedGoogle Scholar
  61. Morse DE, Duncan H, Hooker N, Morse A (1977) Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin endoperoxide synthetase. Science 196:298–300CrossRefPubMedGoogle Scholar
  62. O’Conner C, Mulley JC (1977) Temperature effects on periodicity and embryology, with observations on the population genetics, of the aquacultural echinoid Heliocidaris tuberculata. Aquaculture 12:99–114CrossRefGoogle Scholar
  63. O’Donnell MJ, Todgham AE, Sewell MA, LaTisha MH, Ruggiero K, Fangue NA, Zippay ML, Hofmann GE (2010) Ocean acidification alters skeletogenesis and gene expression in larval sea urchins. Mar Ecol Prog Ser 398:157–171CrossRefGoogle Scholar
  64. Parker LM, Ross PM, O’Connor WA (2009) The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Global Change Biol 15:2123–2136CrossRefGoogle Scholar
  65. Paucellier G, Doree M (1981) Acid release at activation and fertilization of starfish oocytes. Dev Growth Differ 23:287–296CrossRefGoogle Scholar
  66. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel Program Developed for CO2 System Calculations. ORNL/CDIAC-105a. Oak Ridge, Tennessee: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of EnergyGoogle Scholar
  67. Poloczanska ES, Babcock RC, Butler A, Hobday AJ, 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
  68. Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217CrossRefGoogle Scholar
  69. Przeslawski R, Davis AR, Benkendorff K (2005) Synergies, climate change and the development of rocky shore invertebrates. Glob Change Biol 11:515–522CrossRefGoogle Scholar
  70. Przeslawski R, Ahyong S, Byrne M, Worheide G, Hutchings P (2008) Beyond corals and fish: the effects of climate change on non-coral benthic invertebrates of tropical reefs. Global Change Biol 14:2773–2795CrossRefGoogle Scholar
  71. Reuter KE, Lotterhos KE, Crim RN, Thompson CA, Harley CDG (accepted manuscript) Elevated P CO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrous franciscanus. Global Change Biol. doi:10.1111/j.1365-2486.2010.02216.x
  72. Riffell JA, Krug PJ, Zimmer RK (2002) Fertilization in the sea: the chemical identity of an abalone sperm attractant. J Exp Biol 205:1439–1450PubMedGoogle Scholar
  73. Ringwood AH (1992) Comparative sensitivity of gametes and early developmental stages of a sea urchin species (Echinometra mathaei) and a bivalve species (Isognomon californicum) during metal expostures. Arch Environ Contam Toxicol 22:288–295CrossRefPubMedGoogle Scholar
  74. Ringwood AH, Keppler CJ (2002) Water quality variation and clam growth: is pH really a non-issue in estuaries? Estuaries 25:907–910CrossRefGoogle Scholar
  75. Riveros A, Zuñiga M, Larrain A, Becerra J (1996) Relationships between fertilization of the Southeastern Pacific sea urchin Arbacia spatuligera and environmental variables in polluted coastal waters. Mar Ecol Prog Ser 134:159–169CrossRefGoogle Scholar
  76. 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
  77. Selvakumaraswamy P, Byrne M (2000) Reproduction, spawning and development in 5 ophiuroids from Australia and New Zealand. Invertebr Biol 119:394–402CrossRefGoogle Scholar
  78. 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
  79. Smith HW, Clowes GHA (1924) The influence of hydrogen ion concentration on the fertilization process in Arbacia, Asterias and Chaetopterus eggs. Biol Bull 47:333–334CrossRefGoogle Scholar
  80. Song YP, Suquet M, Quéau I, Lebrun L (2009) Setting of a procedure for experimental fertilization of Pacific oyster (Crassostrea gigas) oocytes. Aquaculture 287:311–314CrossRefGoogle Scholar
  81. Styan CA, Byrne M, Franke E (2005) Evolution of egg size and sperm resistance in sea stars: large eggs are not fertilised more readily than small eggs in Patiriella (Echinodermata: Asteroidea). Mar Biol 146:235–242CrossRefGoogle Scholar
  82. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  83. Underwood AJ (1999) Publication of so-called ‘negative’results in marine ecology. Mar Ecol Prog Ser 191:307–309Google Scholar
  84. Ward GE, Brokaw CJ, Garber DL, Vacquier VD (1985) Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J Cell Biol 101P:2324–2329CrossRefGoogle Scholar
  85. Wong E, Davis AR, Byrne M (2010) Reproduction and early development in Haliotis coccoradiata (Vetigastropoda: Haliotidae). Invertebr Reprod Dev (in press)Google Scholar
  86. Wootten JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Natl Acad Sci USA 105:18848–18853CrossRefGoogle Scholar
  87. Yamada K, Mihashi K (1998) Temperature-independent period immediately after fertilization in sea urchin eggs. Biol Bull 195:107–111CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Maria Byrne
    • 1
  • Natalie A. Soars
    • 2
  • Melanie A. Ho
    • 2
  • Eunice Wong
    • 2
  • David McElroy
    • 2
  • Paulina Selvakumaraswamy
    • 2
  • Symon A. Dworjanyn
    • 3
  • Andrew R. Davis
    • 4
  1. 1.Schools of Medical and Biological Sciences, F13University of SydneySydneyAustralia
  2. 2.School of Medical Sciences, F13University of SydneySydneyAustralia
  3. 3.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia
  4. 4.Institute for Conservation BiologyUniversity of WollongongWollongongAustralia

Personalised recommendations