Advertisement

Marine Biology

, 165:96 | Cite as

The effect of warming on mortality, metabolic rate, heat-shock protein response and gonad growth in thermally acclimated sea urchins (Heliocidaris erythrogramma)

  • Januar Harianto
  • Hong Dao Nguyen
  • Sebastian P. Holmes
  • Maria Byrne
Original paper

Abstract

Environmental temperature affects the physiology and fitness of ectotherms, an important consideration in a warming ocean. We investigated the effects of acclimation to increased temperature in the Australian sea urchin, Heliocidaris erythrogramma. After a gradual introduction to increasing temperature (1 °C 6 day−1), sea urchins were held for ~ 3 months in four treatments at three elevated temperatures (22, 24 and 26 °C) and the median annual temperature, 20 °C. The effect of elevated temperature on survival, metabolic rate, Q10, heat-shock protein (HSP70) expression, gonad index and gonad histology were examined. There was no detectable effect of temperature on metabolic rate for the 22 and 24 °C treatments, although survival decreased by 23% in the 24 °C treatment and there was an increase in mean HSP70 expression. At 26 °C, metabolic rate was lower than at 22 and 24 °C, but was similar to controls, indicating that metabolic depression may have occurred, whereas survival decreased by 31% and HSP70 expression increased threefold. It is clear that there is an active physiological response in urchins held at the highest temperatures. The deleterious effect of living at temperatures projected for the future indicates that the persistence of future populations of H. erythrogramma will depend on acclimation as habitat warming continues.

Notes

Acknowledgements

We would like to thank the Sydney Institute of Marine Science (SIMS) for access to facilities. We are grateful to SIMS staff for their help in various matters, and in particular, Joshua Aldridge for his assistance in maintaining the flow-through system. We also sincerely thank the three anonymous reviewers, whose comments helped improve this manuscript substantially. This is SIMS contribution number 223.

Funding

This research was supported by Grants from the NSW Environmental Trust (MB) and the Professor NGW and Mrs Ann Macintosh Memorial Scholarship (JH).

Compliance with ethical standards

Ethical approval

All sea urchins were sampled and treated in accordance with the ethical standards of The University of Sydney, NSW, Australia.

Conflict of interest

All authors have agreed to the submitted version of the manuscript. We have no conflicts of interest to disclose.

Supplementary material

227_2018_3353_MOESM1_ESM.pdf (200 kb)
Supplementary material 1 (PDF 200 kb)
227_2018_3353_MOESM2_ESM.pdf (148 kb)
Supplementary material 2 (PDF 148 kb)
227_2018_3353_MOESM3_ESM.pdf (560 kb)
Supplementary material 3 (PDF 559 kb)

References

  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with imageJ. Biophotonics Int 11:36–41.  https://doi.org/10.1117/1.3589100 CrossRefGoogle Scholar
  2. Anestis A, Lazou A, Portner HO, Michaelidis B (2007) Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. AJP Regul Integr Comp Physiol 293:R911–R921.  https://doi.org/10.1152/ajpregu.00124.2007 CrossRefGoogle Scholar
  3. Angilletta MJ, Huey RB, Frazier MR (2010) Thermodynamic effects on organismal performance: is hotter better? Physiol Biochem Zool 83:197–206.  https://doi.org/10.1086/648567 CrossRefPubMedGoogle Scholar
  4. Bates D, Mächler M, Bolker B, Walker S (2015) fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  5. Branco PC, Borges JCS, Santos MF, Jensch Junior BE, da Silva JRMC (2013) The impact of rising sea temperature on innate immune parameters in the tropical subtidal sea urchin Lytechinus variegatus and the intertidal sea urchin Echinometra lucunter. Mar Environ Res 92:95–101.  https://doi.org/10.1016/j.marenvres.2013.09.005 CrossRefPubMedGoogle Scholar
  6. Brothers CJ, Harianto J, McClintock JB, Byrne M (2016) Sea urchins in a high-CO2 world: the influence of acclimation on the immune response to ocean warming and acidification. Proc R Soc B Biol Sci 283:20161501.  https://doi.org/10.1098/rspb.2016.1501 CrossRefGoogle Scholar
  7. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789.  https://doi.org/10.1890/03-9000 CrossRefGoogle Scholar
  8. Buckley BA, Owen M-E, Hofmann GE (2001) Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J Exp Biol 204:3571–3579PubMedGoogle Scholar
  9. Byrne M, Selvakumaraswamy P, Ho MA, Woolsey E, Nguyen HD (2011) Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Res Part II Top Stud Oceanogr 58:712–719.  https://doi.org/10.1016/j.dsr2.2010.06.010 CrossRefGoogle Scholar
  10. Calosi P, Rastrick SPS, Lombardi C, Guzman HJD, Davidson L, Giangrande A, Hardege JD, Schulze A, Spicer JI, Jahnke M, Gambi M, Giangr A (2013a) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Philos Trans Biol Sci 368:1–15.  https://doi.org/10.1098/rstb.2012.0444 CrossRefGoogle Scholar
  11. Calosi P, Turner LM, Hawkins M, Bertolini C, Nightingale G, Truebano M, Spicer JI (2013b) Multiple physiological responses to multiple environmental challenges: an individual approach. Integr Comp Biol 53:660–670.  https://doi.org/10.1093/icb/ict041 CrossRefPubMedGoogle Scholar
  12. Carey N, Harianto J, Byrne M (2016) Sea urchins in a high CO2 world: partitioned effects of body size, ocean warming and acidification on metabolic rate. J Exp Biol 219:1178–1186.  https://doi.org/10.1242/jeb.136101 CrossRefPubMedGoogle Scholar
  13. Christensen AB, Nguyen HD, Byrne M (2011) Thermotolerance and the effects of hypercapnia on the metabolic rate of the ophiuroid Ophionereis schayeri: inferences for survivorship in a changing ocean. J Exp Mar Biol Ecol 403:31–38.  https://doi.org/10.1016/j.jembe.2011.04.002 CrossRefGoogle Scholar
  14. Clayton ME, Steinmann R, Fent K (2000) Different expression patterns of heat shock proteins hsp 60 and hsp 70 in zebra mussels (Dreissena polymorpha) exposed to copper and tributyltin. Aquat Toxicol 47:213–226.  https://doi.org/10.1016/S0166-445x(99)00022-3 CrossRefGoogle Scholar
  15. Coggan N, Clissold FJ, Simpson SJ (2011) Locusts use dynamic thermoregulatory behaviour to optimize nutritional outcomes. Proc R Soc B Biol Sci 278:2745–2752.  https://doi.org/10.1098/rspb.2010.2675 CrossRefGoogle Scholar
  16. Da Silva J, Cameron JL, Fankboner PV (1986) Movement and orientation patterns in the commercial sea cucumber Parastichopus californicus (Stimpson) (Holothuroidea: Aspidochirotida). Mar Behav Physiol 12:133–147.  https://doi.org/10.1080/10236248609378640 CrossRefGoogle Scholar
  17. Deane EE, Woo NYS (2006) Impact of heavy metals and organochlorines on hsp70 and hsc70 gene expression in black sea bream fibroblasts. Aquat Toxicol 79:9–15.  https://doi.org/10.1016/j.aquatox.2006.04.009 CrossRefPubMedGoogle Scholar
  18. Del Giorgio PA, Williams PJ (eds) (2005) Respiration in aquatic ecosystems. Oxford University Press, OxfordGoogle Scholar
  19. Delorme NJ, Sewell MA (2016) Effects of warm acclimation on physiology and gonad development in the sea urchin Evechinus chloroticus. Comp Biochem Physiol A Mol Integr Physiol 198:33–40.  https://doi.org/10.1016/j.cbpa.2016.03.020 CrossRefPubMedGoogle Scholar
  20. Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–706.  https://doi.org/10.1038/nature09407 CrossRefPubMedGoogle Scholar
  21. Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282CrossRefPubMedGoogle Scholar
  22. Fly EK, Monaco CJ, Pincebourde S, Tullis A (2012) The influence of intertidal location and temperature on the metabolic cost of emersion in Pisaster ochraceus. J Exp Mar Biol Ecol 422–423:20–28.  https://doi.org/10.1016/j.jembe.2012.04.007 CrossRefGoogle Scholar
  23. Fofonoff NP, Millard RC (1983) Algorithms for computation of fundamental properties of seawater. UNESCO Tech Pap Mar Sci 44:53.  https://doi.org/10.1111/j.1365-2486.2005.001000.x CrossRefGoogle Scholar
  24. Franzellitti S, Fabbri E (2005) Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem Biophys Res Commun 336:1157–1163.  https://doi.org/10.1016/j.bbrc.2005.08.244 CrossRefPubMedGoogle Scholar
  25. Garcia-Santos S, Vargas-Chacoff L, Ruiz-Jarabo I, Varela JL, Mancera JM, Fontaínhas-Fernandes A, Wilson JM (2011) Metabolic and osmoregulatory changes and cell proliferation in gilthead sea bream (Sparus aurata) exposed to cadmium. Ecotoxicol Environ Saf 74:270–278.  https://doi.org/10.1016/j.ecoenv.2010.08.023 CrossRefPubMedGoogle Scholar
  26. Gianguzza P, Visconti G, Gianguzza F, Vizzini S, Sarà G, Dupont S (2014) Temperature modulates the response of the thermophilous sea urchin Arbacia lixula early life stages to CO2-driven acidification. Mar Environ Res 93:70–77.  https://doi.org/10.1016/j.marenvres.2013.07.008 CrossRefPubMedGoogle Scholar
  27. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251.  https://doi.org/10.1126/science.1061967 CrossRefPubMedGoogle Scholar
  28. Grambsch PM, Therneau TM (1994) Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 81:515–526.  https://doi.org/10.1093/biomet/81.3.515 CrossRefGoogle Scholar
  29. Guderley H, St-Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205:2237–2249PubMedGoogle Scholar
  30. Gunderson AR, Dillon ME, Stillman JH (2017) Estimating the benefits of plasticity in ectotherm heat tolerance under natural thermal variability. Funct Ecol.  https://doi.org/10.1111/1365-2435.12874 CrossRefGoogle Scholar
  31. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201.  https://doi.org/10.1146/annurev.physiol.67.040403.105027 CrossRefPubMedGoogle Scholar
  32. Hill KL, Rintoul SR, Coleman R, Ridgway KR (2008) Wind forced low frequency variability of the East Australia Current. Geophys Res Lett 35:1–5.  https://doi.org/10.1029/2007GL032912 CrossRefGoogle Scholar
  33. Hobday AJ (2011) Sliding baselines and shuffling species: implications of climate change for marine conservation. Mar Ecol 32:392–403.  https://doi.org/10.1111/j.1439-0485.2011.00459.x CrossRefGoogle Scholar
  34. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, CambridgeGoogle Scholar
  35. Hoekstra LA, Montooth KL (2013) Inducing extra copies of the Hsp70 gene in Drosophila melanogaster increases energetic demand. BMC Evol Biol 13:68.  https://doi.org/10.1186/1471-2148-13-68 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485.  https://doi.org/10.1038/nature09670 CrossRefPubMedGoogle Scholar
  37. Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135.  https://doi.org/10.1016/0169-5347(89)90211-5 CrossRefPubMedGoogle Scholar
  38. Huey RB, Kearney MR, Krockenberger A, Holtum JM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc Lond B Biol Sci 367:1665–1679.  https://doi.org/10.1098/rstb.2012.0005 CrossRefPubMedPubMedCentralGoogle Scholar
  39. IPCC (2013) Climate Change 2013. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  40. IPCC (2014) Climate Change 2014. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Synthesis Report Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  41. Keesing JK (2013) Heliocidaris erythrogramma. In: Developments in aquaculture and fisheries science. Elsevier, Amsterdam, pp 369–379Google Scholar
  42. Kelly MW, Padilla-Gamiño JL, Hofmann GE (2013) Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Glob Change Biol 19:2536–2546.  https://doi.org/10.1111/gcb.12251 CrossRefGoogle Scholar
  43. Kelly NI, Alzaid A, Nash GW, Gamperl AK (2014) Metabolic depression in cunner (Tautogolabrus adspersus) is influenced by ontogeny, and enhances thermal tolerance. PLoS One 9:1–19.  https://doi.org/10.1371/journal.pone.0114765 CrossRefGoogle Scholar
  44. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60–71CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kregel KC (2002) Invited Review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186.  https://doi.org/10.1152/japplphysiol.01267.2001 CrossRefPubMedGoogle Scholar
  46. Laegdsgaard P, Byrne MT, Anderson D (1991) Reproduction of sympatric population of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Mar Biol 110:359–374.  https://doi.org/10.1007/BF01344355 CrossRefGoogle Scholar
  47. Lah RA, Benkendorff K, Bucher D (2017) Thermal tolerance and preference of exploited turbinid snails near their range limit in a global warming hotspot. J Therm Biol 64:100–108.  https://doi.org/10.1016/j.jtherbio.2017.01.008 CrossRefPubMedGoogle Scholar
  48. Lawrence JM (1987) A functional biology of echinoderms. Johns Hopkins University Press, BaltimoreGoogle Scholar
  49. Lenton A, Mcinnes KL, Grady JGO (2015) Marine projections of warming and ocean acidification in the Australasian Region. Aust Meteorol Oceanogr J 65:S1–S28CrossRefGoogle Scholar
  50. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, OxfordCrossRefGoogle Scholar
  51. Logan BR, Wang H, Zhang MJ (2005) Pairwise multiple comparison adjustment in survival analysis. Stat Med 24:2509–2523.  https://doi.org/10.1002/sim.2125 CrossRefPubMedGoogle Scholar
  52. Magozzi S, Calosi P (2015) Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Glob Change Biol 21:181–194.  https://doi.org/10.1111/gcb.12695 CrossRefGoogle Scholar
  53. Marshall DJ, McQuaid CD (2011) Warming reduces metabolic rate in marine snails: adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proc R Soc B Biol Sci 278:281–288.  https://doi.org/10.1098/rspb.2010.1414 CrossRefGoogle Scholar
  54. McElroy DJ, Nguyen HD, Byrne M (2012) Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia. J Exp Mar Biol Ecol 416–417:1–7.  https://doi.org/10.1016/j.jembe.2012.02.003 CrossRefGoogle Scholar
  55. Newell RC, Branch GM (1980) The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv Mar Biol 17:329–396.  https://doi.org/10.1016/S0065-2881(08)60304-1 CrossRefGoogle Scholar
  56. Nguyen KDT, Morley SA, Lai CH, Clark MS, Tan KS, Bates AE, Peck LS (2011) Upper temperature limits of tropical marine ectotherms: global warming implications. PLoS One 6:6–13.  https://doi.org/10.1371/journal.pone.0029340 CrossRefGoogle Scholar
  57. Nguyen HD, Byrne M, Thomson M (2013) Hsp70 expression in the south-eastern Australian sea urchins Heliocidaris erythrogramma and H. tuberculata. Echinoderms Chang World, pp 213–217Google Scholar
  58. O’Connor MI, Piehler MF, Leech DM, Anton A, Bruno JF (2009) Warming and resource availability shift food web structure and metabolism. PLOS Biology 7:e1000178.  https://doi.org/10.1371/journal.pbio.1000178 CrossRefPubMedPubMedCentralGoogle Scholar
  59. O’Donnell MJ, Hammond LM, Hofmann GE (2009) Predicted impact of ocean acidification on a marine invertebrate: elevated CO2 alters response to thermal stress in sea urchin larvae. Mar Biol 156:439–446.  https://doi.org/10.1007/s00227-008-1097-6 CrossRefGoogle Scholar
  60. Osovitz CJ, Hofmann GE (2005) Thermal history-dependent expression of the hsp70 gene in purple sea urchins: biogeographic patterns and the effect of temperature acclimation. J Exp Mar Biol Ecol 327:134–143.  https://doi.org/10.1016/j.jembe.2005.06.011 CrossRefGoogle Scholar
  61. Parry GD (1983) The influence of the cost of growth on ectotherm metabolism. J Theor Biol 101:453–477.  https://doi.org/10.1016/0022-5193(83)90150-9 CrossRefPubMedGoogle Scholar
  62. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496.  https://doi.org/10.1146/annurev.ge.27.120193.002253 CrossRefPubMedGoogle Scholar
  63. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu M-N, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:1–9.  https://doi.org/10.1126/science.aai9214 CrossRefGoogle Scholar
  64. Pinsino A, Matranga V (2015) Sea urchin immune cells as sentinels of environmental stress. Dev Comp Immunol 49:198–205.  https://doi.org/10.1016/j.dci.2014.11.013 CrossRefPubMedGoogle Scholar
  65. Pinsino A, Della Torre C, Sammarini V, Bonaventura R, Amato E, Matranga V (2008) Sea urchin coelomocytes as a novel cellular biosensor of environmental stress: a field study in the Tremiti Island Marine Protected Area, Southern Adriatic Sea, Italy. Cell Biol Toxicol 24:541–552.  https://doi.org/10.1007/s10565-008-9055-0 CrossRefPubMedGoogle Scholar
  66. Poloczanska ES, Burrows MT, Brown CJ, García Molinos J, Halpern BS, Hoegh-Guldberg O, Kappel CV, Moore PJ, Richardson AJ, Schoeman DS, Sydeman WJ (2016) Responses of marine organisms to climate change across oceans. Front Mar Sci 3:62.  https://doi.org/10.3389/fmars.2016.00062 CrossRefGoogle Scholar
  67. Pörtner H (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A Mol Integr Physiol 132:739–761.  https://doi.org/10.1016/S1095-6433(02)00045-4 CrossRefPubMedGoogle Scholar
  68. Pörtner H-O (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893.  https://doi.org/10.1242/jeb.037523 CrossRefPubMedGoogle Scholar
  69. Prosser CL (ed) (1991) Comparative animal physiology, environmental and metabolic animal physiology, part A. Wiley-Liss, New YorkGoogle Scholar
  70. Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Change Biol 21:2122–2140.  https://doi.org/10.1111/gcb.12833 CrossRefGoogle Scholar
  71. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  72. Rich JT, Neely JG, Paniello RC, Voelker CCJ, Nussenbaum B, Wang EW (2010) A practical guide to understanding Kaplan-Meier curves. Otolaryngol Head Neck Surg 143:331–336.  https://doi.org/10.1016/j.otohns.2010.05.007 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Roberts DA, Hofmann GE, Somero GN (1997) Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol Bull 192:309–320.  https://doi.org/10.2307/1542724 CrossRefPubMedGoogle Scholar
  74. RStudio Team (2016) RStudio: integrated development for R. RStudio Inc., BostonGoogle Scholar
  75. Savriama Y, Stige LC, Gerber S, Pérez T, Alibert P, David B (2015) Impact of sewage pollution on two species of sea urchins in the Mediterranean Sea (Cortiou, France): radial asymmetry as a bioindicator of stress. Ecol Indic 54:39–47.  https://doi.org/10.1016/j.ecolind.2015.02.004 CrossRefGoogle Scholar
  76. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5th edn. Cambridge University Press, CambridgeGoogle Scholar
  77. Seebacher F, White CR, Franklin CE (2014) Physiological plasticity increases resilience of ectothermic animals to climate change. Nat Clim Change 5:61–66.  https://doi.org/10.1038/nclimate2457 CrossRefGoogle Scholar
  78. Siikavuopio SI, Mortensen A, Christiansen JS (2008) Effects of body weight and temperature on feed intake, gonad growth and oxygen consumption in green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 281:77–82.  https://doi.org/10.1016/j.aquaculture.2008.05.033 CrossRefGoogle Scholar
  79. Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037.  https://doi.org/10.1046/j.1461-0248.2003.00528.x CrossRefGoogle Scholar
  80. Steneck RS (2013) Sea urchins as drivers of shallow benthic marine community structure. Sea urchins: biology and ecology, 3rd edn. Elsevier, Amsterdam, pp 195–212CrossRefGoogle Scholar
  81. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65.  https://doi.org/10.1126/science.1083073 CrossRefPubMedGoogle Scholar
  82. Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233.  https://doi.org/10.1017/S1464793103006195 CrossRefPubMedGoogle Scholar
  83. Suckling CC, Clark MS, Richard J, Morley SA, Thorne MAS, Harper EM, Peck LS (2015) Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures. J Anim Ecol 84:773–784.  https://doi.org/10.1111/1365-2656.12316 CrossRefPubMedGoogle Scholar
  84. Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686–690.  https://doi.org/10.1038/nclimate1539 CrossRefGoogle Scholar
  85. Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TBH (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125.  https://doi.org/10.1016/j.tree.2013.11.001 CrossRefPubMedGoogle Scholar
  86. Sweet M, Bulling M, Williamson J (2016) New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs. Mar Ecol Prog Ser 551:171–183.  https://doi.org/10.3354/meps11750 CrossRefGoogle Scholar
  87. Terwilliger N, Dumler K (2001) Ontogeny of decapod crustacean hemocyanin: effects of temperature and nutrition. J Exp Biol 204:1013–1020PubMedGoogle Scholar
  88. Vergara J, Silva AX, Manzi C, Nespolo RF, Cardenas L (2017) Differential expression of stress candidate genes for thermal tolerance in the sea urchin Loxechinus albus. J Therm Biol 68:104–109.  https://doi.org/10.1016/j.jtherbio.2017.03.009 CrossRefGoogle Scholar
  89. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172.  https://doi.org/10.1126/science.aad8745 CrossRefPubMedGoogle Scholar
  90. White CR, Kearney MR (2013) Determinants of inter-specific variation in basal metabolic rate. J Comp Physiol B 183:1–26.  https://doi.org/10.1007/s00360-012-0676-5 CrossRefPubMedGoogle Scholar
  91. Whiteley NM, Taylor EW, El Haj AJ (1997) Seasonal and latitudinal adaptation to temperature in crustaceans. J Therm Biol 22:419–427.  https://doi.org/10.1016/S0306-4565(97)00061-2 CrossRefGoogle Scholar
  92. Wood LA, Brown IR, Youson JH (1998) Characterization of the heat shock response in the gills of sea lampreys and a brook lamprey at different intervals of their life cycles. Comp Biochem Physiol A Mol Integr Physiol 120:509–518CrossRefPubMedGoogle Scholar
  93. Yvon-Durocher G, Jones JI, Trimmer M, Woodward G, Montoya JM (2010) Warming alters the metabolic balance of ecosystems. Philos Trans R Soc B Biol Sci 365:2117–2126.  https://doi.org/10.1098/rstb.2010.0038 CrossRefGoogle Scholar
  94. Zar JH (2009) Biostatistical analysis, 5th edn. Pearson, Upper Saddle RiverGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.School of Medical ScienceThe University of SydneySydneyAustralia
  2. 2.School of Life and Environmental SciencesThe University of SydneySydneyAustralia
  3. 3.School of Science and HealthWestern Sydney UniversityPenrithAustralia

Personalised recommendations