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

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Abstract

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.

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References

  • Allen JD, Armstrong AF, Ziegler SL (2015) Environmental induction of polyembryony in echinoid echinoderms. Biol Bull 229:221–231

    Article  PubMed  Google Scholar 

  • 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 9:13

    Article  Google Scholar 

  • 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 155:34–42

    Article  PubMed  Google Scholar 

  • Anger K (2003) Salinity as a key parameter in the larval biology of decapod crustaceans. Invertebr Reprod Dev 43:29–45

    Article  Google Scholar 

  • 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. https://doi.org/10.1093/icb/icu062

    Article  PubMed  Google Scholar 

  • 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 414:28–37

    Article  Google Scholar 

  • 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 542:123–140

    Article  CAS  Google Scholar 

  • Bögner D (2016) Life under climate change scenarios: sea urchins’ cellular mechanisms for reproductive success. J Mar Sci Eng 4:28

    Article  Google Scholar 

  • Bögner D, Bickmeyer U, Köhler A (2014) CO2-induced fertilization impairment in Strongylocentrotus droebachiensis collected in the Arctic. Helgol Mar Res 68:341

    Article  Google Scholar 

  • Burrows MT, Schoeman DS, Richardson AJ, García J (2014) Climate velocity and geographical limits to shifts in species’ distributions. Nature 507:492–495

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1016/j.marenvres.2011.08.008

    Article  CAS  PubMed  Google Scholar 

  • Chan KYK (2012) Biomechanics of larval morphology affect swimming: insights from the sand dollars Dendraster excentricus. Integr Comp Biol 52:458–469

    Article  CAS  PubMed  Google Scholar 

  • 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 138:999–1009

    Article  Google Scholar 

  • Chan KYK, Grünbaum D, Arnberg M, Thorndyke M, Dupont ST (2013) Ocean acidification induces budding in larval sea urchins. Mar Biol 160:2129–2135

    Article  CAS  Google Scholar 

  • Chan KYK, García E, Dupont S (2015) Acidification reduced growth rate but not swimming speed of larval sea urchins. Sci Rep. https://doi.org/10.1038/srep09764

    Google Scholar 

  • 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 223–232

  • 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. https://doi.org/10.1371/journal.pone.0066113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1002/ece3.2317

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:127–143

    Article  Google Scholar 

  • Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1007/s00227-014-2480-0

    Article  CAS  Google Scholar 

  • Delorme NJ, Sewell MA (2016) Genotype-by-environment interactions during early development of the sea urchin Evechinus chloroticus. Mar Biol 163:215. https://doi.org/10.1007/s00227-016-2987-7

    Article  Google Scholar 

  • 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 105:6668–6672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB (2015) Climate change tightens a metabolic constraint on marine habitats. Science 348:1132–1135

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1016/j.aquaculture.2007.07.231

    Article  Google Scholar 

  • Eaves AA, Palmer AR (2003) Reproduction: widespread cloning in echinoderm larvae. Nature 425:146

    Article  CAS  PubMed  Google Scholar 

  • Folt C, Chen C, Moore M, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877

    Article  Google Scholar 

  • 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 163:130

    Article  Google Scholar 

  • 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. https://doi.org/10.1111/j.1440-169X.1994.00275.x

    Article  CAS  Google Scholar 

  • 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 51:119–131

    Article  Google Scholar 

  • 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 319:948–952

    Article  CAS  PubMed  Google Scholar 

  • 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 9:228–241

    Article  PubMed  Google Scholar 

  • Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201

    Article  CAS  PubMed  Google Scholar 

  • 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, Switzerland

  • 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 220:227–233

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1111/gcb.13452

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. https://doi.org/10.1111/j.1440-169X.1992.tb00034.x

    Article  CAS  Google Scholar 

  • Knott KE, Balser EJ, Jaeckle WB, Wray GA (2003) Identification of asteroid genera with species capable of larval cloning. Biol Bull 204:246–255

    Article  CAS  PubMed  Google Scholar 

  • Koehl M, Cooper T (2015) Swimming in an unsteady world. Integr Comp Biol 55:683–697. https://doi.org/10.1093/icb/icv092

    Article  CAS  PubMed  Google Scholar 

  • 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 388:137–146

    Article  Google Scholar 

  • Lee T, Leung W, Ginn E (2008) Rainfall projections for Hong Kong based on the IPCC fourth assessment report. Hong Kong Meteorol Soc Bull 18:12–22

    Google Scholar 

  • Lu X, Wu R (2005) UV induces reactive oxygen species, damages sperm, and impairs fertilisation in the sea urchin Anthocidaris crassispina. Mar Biol 148:51–57

    Article  CAS  Google Scholar 

  • Mao J-Q, Wong KT, Lee JH, Choi K (2011) Tidal flushing time of marine fish culture zones in Hong Kong. China Ocean Eng 25:625–643

    Article  Google Scholar 

  • 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. https://doi.org/10.1006/dbio.1997.8585

    Article  CAS  PubMed  Google Scholar 

  • McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: animal loss in the global ocean. Science 347:1255641

    Article  PubMed  Google Scholar 

  • Metaxas A (1998) The effect of salinity on larval survival and development in the sea urchin Echinometra lucunter. Invertebr Reprod Dev 34:323–330. https://doi.org/10.1080/07924259.1998.9652667

    Article  Google Scholar 

  • Metaxas A, Young CM (1998) Behaviour of echinoid larvae around sharp haloclines: effects of the salinity gradient and dietary conditioning. Mar Biol 131:443–459

    Article  CAS  Google Scholar 

  • 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 68:195–199

    Article  PubMed  Google Scholar 

  • Okazaki K (1956) Exogastrulation induced by calcium deficiency in the sea urchin, Pseudocentrotus depressus. Dev Growth Differ 3:23–36

    Article  Google Scholar 

  • 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 212:151–160

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 188:123–132

    Article  Google Scholar 

  • 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. https://doi.org/10.1139/z85-227

    Article  Google Scholar 

  • 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 116:583–591

    Article  Google Scholar 

  • 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 21:4547–4562

    Article  CAS  PubMed  Google Scholar 

  • 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 9:676–682

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1007/s00338-016-1505-1

    Article  Google Scholar 

  • 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, Seattle

    Google Scholar 

  • Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881. https://doi.org/10.1371/journal.pone.0022881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi T, Hoshi M, Asahina É (1977) Exogastrulation induced by chilling in sea urchin larvae. Dev Growth Differ 19:131–137

    Article  Google Scholar 

  • Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539–544

    Article  PubMed  Google Scholar 

  • Tomanek L, Helmuth B (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integr Comp Biol 42:771–775

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1016/j.rsma.2016.03.005

    Article  Google Scholar 

  • 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 38:1097–1104

    Article  CAS  Google Scholar 

  • Vaughn D (2009) Predator-induced larval cloning in the sand dollar Dendraster excentricus: might mothers matter? Biol Bull 217:103–114

    Article  PubMed  Google Scholar 

  • 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 157:1301–1312

    Article  Google Scholar 

  • 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 199:298–304

    Article  CAS  PubMed  Google Scholar 

  • 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 324:141–156

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1111/j.1432-1033.1995.0515n.x

    Article  CAS  PubMed  Google Scholar 

  • 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 Kong

    Book  Google Scholar 

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Acknowledgements

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.

Funding

This study is supported by the Research Grant Council, University Grants Committee, Hong Kong (Project no. 26102515) to KC and partially supported by the Croucher Foundation, Hong Kong.

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Authors and Affiliations

  1. Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China

    Karen Kiu-Yan Mak & Kit Yu Karen Chan

  2. Department of Microbiology and Immunology, Faculty of Science, University of British Columbia, Vancouver, Canada

    Karen Kiu-Yan Mak

  3. Department of Earth, Ocean and Atmospheric Sciences, Faculty of Science, University of British Columbia, Vancouver, Canada

    Karen Kiu-Yan Mak

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  1. Karen Kiu-Yan Mak
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Correspondence to Kit Yu Karen Chan.

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Mak, K.KY., Chan, K.Y.K. Interactive effects of temperature and salinity on early life stages of the sea urchin Heliocidaris crassispina. Mar Biol 165, 57 (2018). https://doi.org/10.1007/s00227-018-3312-4

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