Marine Biology

, 165:57 | Cite as

Interactive effects of temperature and salinity on early life stages of the sea urchin Heliocidaris crassispina

Original paper


Marine organisms are currently challenged by multiple and interactive environmental stressors. In the subtropics, warming and intensified precipitation, and hence, reduced salinity, are particularly relevant. Using the sea urchin, Heliocidaris crassispina, we investigated the effects of warming and low salinity on fertilization success and early development. These planktonic developmental stages play significant roles in shaping population dynamics. Gametes were exposed to a temperature gradient (28–43 °C) while being held at two salinities (24 and 32). Fertilization had a higher critical temperature (LT50), the temperature at which 50% individuals reached the designated stage, of 39 °C than that of blastula formation at 31 °C for both salinities, suggesting between-stage variations in sensitivity. The LT50 for blastula formation was very close to present-day recorded maximum sea surface temperature of 31 °C suggesting a small thermal safety factor. Larvae were also reared to the eight-arm stage in one of the four combinations of temperatures (24 and 28 °C) and salinities (24 and 32), which correspond to sea surface temperatures and salinities observed during the urchin’s spawning season. Low salinity and high temperature had interactive effects in reducing larval survivorship. However, amongst larvae that survived the combined stress, warming reduced the negative impact of reduced salinity on arm growth. Unexpected release of blastula-like particles was documented in all treatments except the control (24 °C and salinity 32). Incomplete separations that resulted in conjoined twins, however, were only found at 28 °C. There were significantly different responses in fertilization success and larval growth between maternal lineages. Such intra-specific variations highlight the presence of phenotypic plasticity and could imply the presence of genetic variations in response to thermal and salinity stress. Such plasticity suggests that although purple urchins are experiencing extreme conditions that are stressful at present, they may be able to cope with the future ocean conditions.



We thank the reviewers for their inputs, Y. K. Tam and L. W. Pang for their technical assistance during this study, C. Yau, N. Dorey and J. Ngo for their input on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2018_3312_MOESM1_ESM.docx (86 kb)
Supplementary material 1 (DOCX 86 kb)


  1. Allen JD, Armstrong AF, Ziegler SL (2015) Environmental induction of polyembryony in echinoid echinoderms. Biol Bull 229:221–231CrossRefPubMedGoogle Scholar
  2. Allen J, Schrage K, Foo S, Watson S-A, Byrne M (2017) The effects of salinity and pH on fertilization, early development, and hatching in the crown-of-thorns seastar. Diversity 9:13CrossRefGoogle Scholar
  3. An MI, Choi CY (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comp Biochem Physiol B Biochem Mol Biol 155:34–42CrossRefPubMedGoogle Scholar
  4. Anger K (2003) Salinity as a key parameter in the larval biology of decapod crustaceans. Invertebr Reprod Dev 43:29–45CrossRefGoogle Scholar
  5. Applebaum SL, Pan TCF, Hedgecock D, Manahan DT (2014) Separating the nature and nurture of the allocation of energy in response to global change. Integr Comp Biol 54:284–295. CrossRefPubMedGoogle Scholar
  6. Arellano SM, Reitzel AM, Button CA (2012) Variation in vertical distribution of sand dollar larvae relative to haloclines, food, and fish cues. J Exp Mar Biol Ecol 414:28–37CrossRefGoogle Scholar
  7. Bashevkin SM, Lee D, Driver P, Carrington E, George SB (2016) Prior exposure to low salinity affects the vertical distribution of Pisaster ochraceus (Echinodermata: Asteroidea) larvae in haloclines. Mar Ecol Prog Ser 542:123–140CrossRefGoogle Scholar
  8. Bögner D (2016) Life under climate change scenarios: sea urchins’ cellular mechanisms for reproductive success. J Mar Sci Eng 4:28CrossRefGoogle Scholar
  9. Bögner D, Bickmeyer U, Köhler A (2014) CO2-induced fertilization impairment in Strongylocentrotus droebachiensis collected in the Arctic. Helgol Mar Res 68:341CrossRefGoogle Scholar
  10. Burrows MT, Schoeman DS, Richardson AJ, García J (2014) Climate velocity and geographical limits to shifts in species’ distributions. Nature 507:492–495CrossRefPubMedGoogle Scholar
  11. Carballeira C, Martín-Díaz L, DelValls TA (2011) Influence of salinity on fertilization and larval development toxicity tests with two species of sea urchin. Mar Environ Res 72:196–203. CrossRefPubMedGoogle Scholar
  12. Chan KYK (2012) Biomechanics of larval morphology affect swimming: insights from the sand dollars Dendraster excentricus. Integr Comp Biol 52:458–469CrossRefPubMedGoogle Scholar
  13. Chan BKK, Morritt D, Williams GA (2001) The effect of salinity and recruitment on the distribution of Tetraclita squamosa and Tetraclita japonica (Cirripedia; Balanomorpha) in Hong Kong. Mar Biol 138:999–1009CrossRefGoogle Scholar
  14. Chan KYK, Grünbaum D, Arnberg M, Thorndyke M, Dupont ST (2013) Ocean acidification induces budding in larval sea urchins. Mar Biol 160:2129–2135CrossRefGoogle Scholar
  15. Chan KYK, García E, Dupont S (2015) Acidification reduced growth rate but not swimming speed of larval sea urchins. Sci Rep. Google Scholar
  16. Chiu S (1985) Feeding biology of the short-spined sea urchin Anthocidaris crassispina. In: Agassiz A (ed) Hong Kong proceedings of the fifth international echinoderm conference Balkema, Boston, pp 223–232Google Scholar
  17. Ciapa B, Philippe L (2013) Intracellular and extracellular pH and Ca are bound to control mitosis in the early sea urchin embryo via ERK and MPF activities. PLoS One 8:e66113. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Collin R, Chan KYK (2016) The sea urchin Lytechinus variegatus lives close to the upper thermal limit for early development in a tropical lagoon. Ecol Evol 6:5623–5634. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Craig SF, Slobodkin LB, Wray GA, Biermann CH (1997) The ‘paradox’of polyembryony: a review of the cases and a hypothesis for its evolution. Evol Ecol 11:127–143CrossRefGoogle Scholar
  20. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315CrossRefPubMedGoogle Scholar
  21. Delorme NJ, Sewell MA (2014) Temperature and salinity: two climate change stressors affecting early development of the New Zealand sea urchin Evechinus chloroticus. Mar Biol 161:1999–2009. CrossRefGoogle Scholar
  22. Delorme NJ, Sewell MA (2016) Genotype-by-environment interactions during early development of the sea urchin Evechinus chloroticus. Mar Biol 163:215. CrossRefGoogle Scholar
  23. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672CrossRefPubMedPubMedCentralGoogle Scholar
  24. Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB (2015) Climate change tightens a metabolic constraint on marine habitats. Science 348:1132–1135CrossRefPubMedGoogle Scholar
  25. Ding J, Chang Y, Wang C, Cao X (2007) Evaluation of the growth and heterosis of hybrids among three commercially important sea urchins in China: Strongylocentrotus nudus, S. intermedius and Anthocidaris crassispina. Aquaculture 272:273–280. CrossRefGoogle Scholar
  26. Eaves AA, Palmer AR (2003) Reproduction: widespread cloning in echinoderm larvae. Nature 425:146CrossRefPubMedGoogle Scholar
  27. Folt C, Chen C, Moore M, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877CrossRefGoogle Scholar
  28. Foo SA, Sparks KM, Uthicke S, Karelitz S, Barker M, Byrne M, Lamare M (2016) Contributions of genetic and environmental variance in early development of the Antarctic sea urchin Sterechinus neumayeri in response to increased ocean temperature and acidification. Mar Biol 163:130CrossRefGoogle Scholar
  29. Fujita Y, Yamasu K, Suyemitsu T, Ishihara K (1994) A protein that binds an exogastrula-inducing peptide, EGIP-D, in the hyaline layer of sea urchin embryos. Dev Growth Differ 36:275–280. CrossRefGoogle Scholar
  30. Greenwood P, Bennett T (1981) Some effects of temperature-salinity combinations on the early development of the sea urchin Parechinus angulosus (Leske). Fertilization. J Exp Mar Biol Ecol 51:119–131CrossRefGoogle Scholar
  31. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE (2008) A global map of human impact on marine ecosystems. Science 319:948–952CrossRefPubMedGoogle Scholar
  32. Harley CD, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJ, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241CrossRefPubMedGoogle Scholar
  33. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201CrossRefPubMedGoogle Scholar
  34. IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, SwitzerlandGoogle Scholar
  35. Ishihara K, Tonegawa Y, Suyemitsu T, Kubo H (1982) The blastocoelic fluid of sea urchin embryo induces exogastrulation. J Exp Zool Part A Ecol Genet Physiol 220:227–233CrossRefGoogle Scholar
  36. Karelitz SE, Uthicke S, Foo SA, Barker MF, Byrne M, Pecorino D, Lamare MD (2017) Ocean acidification has little effect on developmental thermal windows of echinoderms from Antarctica to the tropics. Glob Change Biol 23:657–672. CrossRefGoogle Scholar
  37. 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 19:2536–2546CrossRefGoogle Scholar
  38. Kinoshita K, Fujii Y, Fujita Y, Yamasu K, Suyemitsu T, Ishihara K (1992) Maternal exogastrula-inducing peptides (EGIPs) and their changes during development in the sea urchin Anthocidaris crassispina. Dev Growth Differ 34:661–668. CrossRefGoogle Scholar
  39. Knott KE, Balser EJ, Jaeckle WB, Wray GA (2003) Identification of asteroid genera with species capable of larval cloning. Biol Bull 204:246–255CrossRefPubMedGoogle Scholar
  40. Koehl M, Cooper T (2015) Swimming in an unsteady world. Integr Comp Biol 55:683–697. CrossRefPubMedGoogle Scholar
  41. Kuo ES, Sanford E (2009) Geographic variation in the upper thermal limits of an intertidal snail: implications for climate envelope models. Mar Ecol Prog Ser 388:137–146CrossRefGoogle Scholar
  42. Lee T, Leung W, Ginn E (2008) Rainfall projections for Hong Kong based on the IPCC fourth assessment report. Hong Kong Meteorol Soc Bull 18:12–22Google Scholar
  43. Lu X, Wu R (2005) UV induces reactive oxygen species, damages sperm, and impairs fertilisation in the sea urchin Anthocidaris crassispina. Mar Biol 148:51–57CrossRefGoogle Scholar
  44. Mao J-Q, Wong KT, Lee JH, Choi K (2011) Tidal flushing time of marine fish culture zones in Hong Kong. China Ocean Eng 25:625–643CrossRefGoogle Scholar
  45. Matese JC, Black S, McClay DR (1997) Regulated exocytosis and sequential construction of the extracellular matrix surrounding the sea urchin zygote. Dev Biol 186:16–26. CrossRefPubMedGoogle Scholar
  46. McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: animal loss in the global ocean. Science 347:1255641CrossRefPubMedGoogle Scholar
  47. Metaxas A (1998) The effect of salinity on larval survival and development in the sea urchin Echinometra lucunter. Invertebr Reprod Dev 34:323–330. CrossRefGoogle Scholar
  48. Metaxas A, Young CM (1998) Behaviour of echinoid larvae around sharp haloclines: effects of the salinity gradient and dietary conditioning. Mar Biol 131:443–459CrossRefGoogle Scholar
  49. Morley S, Nguyen K, Peck L, Lai C-H, Tan K (2016) Can acclimation of thermal tolerance, in adults and across generations, act as a buffer against climate change in tropical marine ectotherms? J Therm Biol 68:195–199CrossRefPubMedGoogle Scholar
  50. Okazaki K (1956) Exogastrulation induced by calcium deficiency in the sea urchin, Pseudocentrotus depressus. Dev Growth Differ 3:23–36CrossRefGoogle Scholar
  51. Pechenik JA, Pearse JS, Qian P-Y (2007) Effects of salinity on spawning and early development of the tube-building polychaete Hydroides elegans in Hong Kong: not just the sperm’s fault? Biol Bull 212:151–160CrossRefPubMedGoogle Scholar
  52. 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 21:2122–2140CrossRefGoogle Scholar
  53. Qiu J-W, Qian P-Y (1999) Tolerance of the barnacle Balanus amphitrite amphitrite to salinity and temperature stress: effects of previous experience. Mar Ecol Prog Ser 188:123–132CrossRefGoogle Scholar
  54. Roller RA, Stickle WB (1985) Effects of salinity on larval tolerance and early developmental rates of four species of echinoderms. Can J Zool 63:1531–1538. CrossRefGoogle Scholar
  55. Roller RA, Stickle WB (1993) Effects of temperature and salinity acclimation of adults on larval survival, physiology, and early development of Lytechinus variegatus (Echinodermata: Echinoidea). Mar Biol 116:583–591CrossRefGoogle Scholar
  56. Runcie DE, Garfield DA, Babbitt CC, Wygoda JA, Mukherjee S, Wray GA (2012) Genetics of gene expression responses to temperature stress in a sea urchin gene network. Mol Ecol 21:4547–4562CrossRefPubMedGoogle Scholar
  57. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMedGoogle Scholar
  58. Sparks KM, Foo SA, Uthicke S, Byrne M, Lamare M (2017) Paternal identity influences response of Acanthaster planci embryos to ocean acidification and warming. Coral Reefs 36:325–338. CrossRefGoogle Scholar
  59. Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, SeattleGoogle Scholar
  60. Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Takahashi T, Hoshi M, Asahina É (1977) Exogastrulation induced by chilling in sea urchin larvae. Dev Growth Differ 19:131–137CrossRefGoogle Scholar
  62. Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539–544CrossRefPubMedGoogle Scholar
  63. Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integr Comp Biol 42:771–775CrossRefPubMedGoogle Scholar
  64. Urriago JD, Wong JCY, Dumont CP, Qiu J-W (2016) Reproduction of the short-spined sea urchin Heliocidaris crassispina (Echinodermata: Echinoidea) in Hong Kong with a subtropical climate. Reg Stud Mar Sci 8:445–453. CrossRefGoogle Scholar
  65. Vaschenko M, Zhang Z, Lam P, Wu R (1999) Toxic effects of cadmium on fertilizing capability of spermatozoa, dynamics of the first cleavage and pluteus formation in the sea urchin Anthocidaris crassispina (Agassiz). Mar Pollut Bull 38:1097–1104CrossRefGoogle Scholar
  66. Vaughn D (2009) Predator-induced larval cloning in the sand dollar Dendraster excentricus: might mothers matter? Biol Bull 217:103–114CrossRefPubMedGoogle Scholar
  67. Vaughn D (2010) Why run and hide when you can divide? Evidence for larval cloning and reduced larval size as an adaptive inducible defense. Mar Biol 157:1301–1312CrossRefGoogle Scholar
  68. Vickery MS, McClintock JB (2000) Effects of food concentration and availability on the incidence of cloning in planktotrophic larvae of the sea star Pisaster ochraceus. Biol Bull 199:298–304CrossRefPubMedGoogle Scholar
  69. Wai T-C, Williams GA (2005) The relative importance of herbivore-induced effects on productivity of crustose coralline algae: sea urchin grazing and nitrogen excretion. J Exp Mar Biol Ecol 324:141–156CrossRefGoogle Scholar
  70. Yamasu K, Watanabe H, Kohchi C, Soma G-I, Mizuno D-I, Akasaka K, Shimada H, Suyemitsu T, Ishihara K (1995) Molecular cloning of a cDNA that encodes the precursor to several exogastrula-inducing peptides, epidermal-growth-factor-related polypeptides of the sea urchin Anthocidaris crassispina. Eur J Biochem 228:515–523. CrossRefPubMedGoogle Scholar
  71. Zhao B (2002) Larval biology and ecology of a non-indigenous species, the slipper limpet Crepidula onyx. The Hong Kong University of Science and Technology, Hong KongCrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Division of Life ScienceThe Hong Kong University of Science and TechnologyHong KongChina
  2. 2.Department of Microbiology and Immunology, Faculty of ScienceUniversity of British ColumbiaVancouverCanada
  3. 3.Department of Earth, Ocean and Atmospheric Sciences, Faculty of ScienceUniversity of British ColumbiaVancouverCanada

Personalised recommendations