Skip to main content

Advertisement

SpringerLink
Log in

Developing in the intertidal: effects of salinity and temperature on development to the pentameral juvenile seastar, Parvulastra exigua

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

For intertidal marine species, salinity and temperature are important environmental factors with conditions ranging from oceanic salinity and temperature at high tide to almost freshwater conditions due to rain accompanied by aerial temperature exposure at low tide. The interactive effects of these stressors across development to the juvenile is not known. We investigated the impacts of salinity (29–41 ppt) and temperature (20°–24 ℃) on holobenthic intertidal development to the five-armed juvenile asterinid seastar Parvulastra exigua. There was an interaction between the stressors with highest mortality in the high salinity and temperature (38 ppt, 41 ppt, 24 ℃) treatments. Developmental stage progression was enhanced by increased temperature. On day 1, there was an interaction between salinity and temperature on developmental stage progression, where high salinity (41 ppt) retarded development at the control temperature (20 ℃). The juveniles reared at 24 ℃ were smaller than those at cooler temperatures, suggesting application of the temperature size rule. The low (29 ppt) and high (38 ppt, 41 ppt) salinity treatments produced the smallest and largest juveniles, respectively. In the 35 ppt and 38 ppt salinity conditions at 20 ℃, most juveniles had the normal five-armed profile. Body plan development was perturbed with deviations from pentamery at 29 ppt, 32 ppt and 41 ppt and at 22 ℃ and 24 ℃ in formation of no armed juveniles and ones with abnormal arm number (4, 6, 7 arms). Normal development at 35–38 ppt and 20–22 ℃ reflects breeding period conditions. Prolonged exposure to low and high salinity and increased temperature is deleterious to development in P. exigua and alters body morphology with implications for function and survival.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data and material availability

Available on request.

References

  • Abdel-Raheem ST, Allen JD (2019) Developmental consequences of temperature and salinity stress in the sand dollar Dendraster excentricus. Biol Bull 237:227–240

    CAS  PubMed  Google Scholar 

  • Angilletta MJ, Steury T, Sears MW (2004) Temperature, growth rate and body size in ectotherms: fitting pieces of a life-history puzzle. Integ Comp Biol 44:498–509

    Google Scholar 

  • Asha PS, Muthiah P (2005) Effects of temperature, salinity and pH on larval growth, survival and development of the sea cucumber Holothuria spinifera Theel. Aquaculture 250:823–829

    CAS  Google Scholar 

  • Ashcroft L, Karoly DJ, Dowdy AJ (2019) Historical extreme rainfall events in southeastern Australia. Weather Clim Extrem 25:100210

    Google Scholar 

  • Babcock RC, Bustamante RH, Fulton EA, Fulton DJ, Haywood MDE, Hobday AJ, Kenyon R, Matear RJ, Plagányi EE, Richardson A, Vanderklift MA (2019) Severe continental-scale impacts of climate change are happening now: extreme climate events impact marine habitat forming communities along 45% of Australia’s Coast. Front Mar Sci 6:411

    Google Scholar 

  • Balogh R (2019) Impact of environmental stressors on development to the pentamerous five armed juvenile in the starfish, Parvulastra exigua. Honours thesis. University of Sydney, Australia

  • Balogh R, Byrne M (2020) Developing in a warming intertidal, negative carry over effects of heatwave conditions in development to the pentameral starfish in Parvulastra exigua. Mar Environ Res 162:105083

    CAS  PubMed  Google Scholar 

  • Barker MF, Russell MP (2008) The distribution and behaviour of Patiriella mortenseni and P. regularis in the extreme hyposaline conditions of the southern New Zealand fiords. J Exp Mar Biol Ecol 335:76–84

    Google Scholar 

  • Byrne M (1992) Reproduction of sympartric populations of Patiriella gunnii, M. calcar and P. exigua in New South wales, asterinid seastars with direct development. Mar Biol 114:297–316

    Google Scholar 

  • Byrne M (1995) Changes in larval morphology in the evolution of benthic development by Patiriella exigua (Asteroidea: Asterinindae), a comparison with the larvae of Patiriella species with planktonic development. Biol Bull 188:293–305

    CAS  PubMed  Google Scholar 

  • 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. Oceanogr Mar Biol 49:1–42

    Google Scholar 

  • Carballeira C, Martin-Diaz L, DelValls TA (2011) Influence of salinity on fertilisation and larval development toxicity tests with two species of sea urchin. Mar Environ Res 72:196–203

    CAS  PubMed  Google Scholar 

  • Cerra A, Byrne M (1995) Structure of the extraembryonic matricies around the benthic embryos of Patiriella exigua (Asteroidea) and their roles in benthic development: comparison with the planktonic embryos of Patiriella regularis. J Morphol 225:77–89

    PubMed  Google Scholar 

  • Clarke KE (1988) The roles of heredity, osmotic stress, and regeneration in non-pentamerous symmetry in Patiria miniata. In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Echinoderm biology. Balkema, Rotterdam, p 792

    Google Scholar 

  • Clements M, Wolfe K, Schwartz K, Byrne M (2019) Forever fissiparous: asexual propagation and stable demography in a tropical and geographically isolated asterinid sea star. Mar Biol 166:1–11

    Google Scholar 

  • Cowart DA, Ulrich PN, Miller DC, Marsh AG (2009) Salinity sensitivity of early embryos of the Antarctic sea urchin, Sterechinus nuemayeri. Polar Biol 32:435–441

    Google Scholar 

  • Dartnall AJ (1971) Australian sea stars of the genus Patiriella (Asteroidea, Asterinidae). Proc Linn Soc NSW 96:39–51

    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

    CAS  Google Scholar 

  • Ehlinger GS, Tankersley RA (2004) Survival and development of horseshoe crab (Limulus polyphemus) embryos and larvae in hypersaline conditions. Biol Bull 206:87–94

    PubMed  Google Scholar 

  • Fell HB (1962) West-wind drift dispersal of echinoderms in the southern hemisphere. Nature 193:759–761

    Google Scholar 

  • García E, Clemente S, Hernández JC (2018) Effects of natural current pH variability on the sea urchin Paracentrotus lividus larvae development and settlement. Mar Environ Res 139:11–18

    PubMed  Google Scholar 

  • Glockner-Fagetti A, Phillips NE (2019) Low salinity and sediment stress on sea urchin Evechinus chloroticus larvae has latent effects on juvenile performance. Mar Ecol Prog Ser 619:85–96

    Google Scholar 

  • Gosselin L, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282

    Google Scholar 

  • Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci 104:1745–1750

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hart MW, Keever CC, Dartnall AJ, Byrne M (2006) Morphological and genetic variation in dicate cryptic species within Lamarck’s little sea star, Parvulastra (= Patiriella) exigua. Biol Bull 210:158–167. https://doi.org/10.2307/4134604

    Article  CAS  PubMed  Google Scholar 

  • Held MBE, Harley CDG (2009) Response to low salinity by the sea star Pisaster ochraceus from high- and low-salinity populations. Invertebr Biol 128(4):381–390

    Google Scholar 

  • Hotchkiss F (2000) On the number of rays in starfish. Am Zool 40:340–354

    Google Scholar 

  • IPCC (2019) Summary for policymakers. In: Shukla PR, Skea J, Calvo Buendia E, Masson-Delmotte V, Pörtner H-O, Roberts DC, Zhai P, Slade R, Connors S, van Diemen S, Ferrat M, Haughey E, Luz S, Neogi S, Pathak M, Petzold J, Portugal Pereira J, Vyas P, Huntley E, Kissick K, Belkacemi M, Malley J (eds) Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems

  • Khan M, Whittington C, Thompson M, Byrne M (2019) Intragonadal incubation of progeny in three viviparous asterinid sea stars that differ in offspring provisioning, lecithotrophy vs matrotrophy. Mar Biol 166:1–17

    Google Scholar 

  • Kashenko SD (2006) Responses of embryos and larvae of the starfish Asterinas amerensis to changes in temperature and salinity. Russ J Mar Biol 31:294–302

    Google Scholar 

  • Lawrence JM (1975) The effect of temperature-salinity combinations on the functional well-being of the adult Lytechius variegatus (Lamarck) (Echinodermata, Echinoidea). J Exp Mar Biol Ecol 18:271–275

    Google Scholar 

  • Mak KK-Y, Chan KYK (2018) Interactive effects of temperature and salinity on early life stages of the sea urchin Heliocidaris crassispina. Mar Biol 165:57

    Google Scholar 

  • Marsh AG, Watts SA, Chen CP, McClintock JB (1986) The effect of high salinity on development, mortality and ray number of Echinaster spinulosus (Echinodermata: Asteroidea) at different developmental stages. Comp Biochem Phys 88:229–231

    Google Scholar 

  • Marthy HJ (1980) Etude descriptive du developpement de loef d’Asterina (Echinoderme, Asteride) son interet en embryologie experimentale. Vie Milieu 30:75–80

    Google Scholar 

  • Martinez A, Queiroz E, Bryson M, Byrne M, Coleman R (2016) Incorporating in situ habitat patchiness in site selection models reveals that site fidelity is not always a consequence of animal choice. J Anim Ecol 86:847–856

    Google Scholar 

  • Montory JA, Pechenik JA, Diederich CM, Chaparro OR (2014) Effects of low salinity on adult behavior and larval performance in the intertidal gastropod Crepipatella peruviana (Calyptraeidae). PLoS ONE 9(7):e103820

    PubMed  PubMed Central  Google Scholar 

  • Nasrolahi A, Pansch C, Lenz M, Wahl M (2013) Temperature and salinity interactively impact early juvenile development: a bottleneck in barnacle ontogeny. Mar Biol 160:1109–1117

    Google Scholar 

  • Nguyen HD, Doo SS, Soars NA, Byrne M (2012) Non-calcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star Meridiastra calcar. Global Change Biol 18:2466–2476

    Google Scholar 

  • Nguyen HD, Byrne M (2014) Early benthic juvenile Parvulastra exigua (Asteroidea) are tolerant to extreme acidification and warming in its intertidal habitat. J Exp Mar Biol Ecol 453:36–42

    CAS  Google Scholar 

  • Oliver ECJ, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Gupta AS, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SE, Scannell HA, Straub SC, Wernberg T (2018) Long and more frequent marine heatwaves over the past century. Nat Commun 9:1–12

    CAS  Google Scholar 

  • Payne NL, Smith JA, van der Meulen DE, Taylor MD, Watanabe YY, Takahashi A, Marzullo TA, Gray CA, Cadiou G, Suthers IM (2016) Temperature dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance. Funct Ecol 30:903–912

    Google Scholar 

  • Pechenik JA, Wendt DE, Jarrett JN (1998) Metamorphosis is not a new beginning. Bioscience 48:901–910

    Google Scholar 

  • Pechenik JA (2018) Latent effects: surprising consequences of embryonic and larval experience on life after metamorphosis. In: Carrier TJ, Reitzel AM, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, Oxford, pp 208–225

    Google Scholar 

  • Pia TS, Johnson T, George S (2012) Salinity induced morphological changes in Pisaster ochraceus (Echinodermata: Asteroidea) larvae. J Plank Res 34:590–601

    CAS  Google Scholar 

  • Przeslawski R (2004) A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Res 24:43–63

    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

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Roller SA, Stickle WB (1984) Effects of salinity on larval tolerance and early developmental rates of four species of echinoderms. Can J Zool 63:1531–1538

    Google Scholar 

  • Roller SA, 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

    Google Scholar 

  • Rose R (1986) Direct development in Rostanga arbutus (Angas) (Mollusca: Nudibranchia) and the effects of temperature and salinity on embryos reared in the laboratory. J Malacol Soc Aust 7(3–4):141–154

    Google Scholar 

  • Russell MP (2013) Echinoderm responses to variation in salinity. Adv Mar Biol 66:171–212

    PubMed  Google Scholar 

  • Sheppard Brennand H, Soars N, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5:e11372

    PubMed  PubMed Central  Google Scholar 

  • Smale DA, Werberg T, Oliver ECJ, Thomsen M, Harvey BP, Straub SC, Burrows MT, Alexander LV, Benthuysen JA, Donat MG, Feng M, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SEP, Scanell HA, Gupta AS, Payne BL, Moore PJ (2019) Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Natl Clim Change 9:306–312

    Google Scholar 

  • Stickle WB, Diehl WJ (1987) Effects of salinity on echinoderms. In: Lawrence JM, Jangoux M (eds) Echinoderm studies, vol 2. Balkema, Rotterdam, pp 235–285

    Google Scholar 

  • Thiyagarajan V, Harder T, Qian P-Y (2003) Combined effects of temperature and salinity on larval development and attachment of the subtidal barnacle Balanus trigonus Darwin. J Exp Mar Biol Ecol 287:223–236

    Google Scholar 

  • Trowbridge CD (1994) Life at the edge: population dynamics and salinity tolerance of a high intertidal, pool-dwelling ascoglassan opisthobranch on the New Zealand rocky shores. J Exp Mar Biol Ecol 182:65–84

    Google Scholar 

  • Watts SA, Scheilbling RE, Marsh AG, McClintock JB (1983) Induction of aberrant ray numbers in Echinaster sp. (Echinodermata: Asteroidea). Fla Sci 46:125–128

    Google Scholar 

  • Wolfe K, Nguyen HD, Davey M, Byrne M (2020) Characterising biogeochemical fluctuations in a world of extremes: a synthesis for temperate intertidal habitats in the face of global change. Glob Change Biol 26(7):3858–3879

    Google Scholar 

Download references

Acknowledgements

This research was supported by an Australian Research Council Grant (DP150102771). We thank the reviewers for insightful comments that improved the manuscript. Thanks to J. Lin, M. Rayhanna and A. Henning for assistance with measuring and photography of juveniles. This is SIMS contribution number 275 of the Sydney Institute of Marine Science.

Funding

This research was supported by an Australian Research Council Grant (DP150102771).

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, A11, The University of Sydney, Camperdown, NSW, 2006, Australia

    Regina Balogh & Maria Byrne

Authors
  1. Regina Balogh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Byrne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Regina Balogh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Ethics approval was not required for this project.

Consent to participate

Authors agree to participate in the publication of this manuscript.

Consent for publication

Authors give consent to the publication of this manuscript.

Additional information

Responsible Editor: A.E. Todgham.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by: K. Chan, M. P. Russell and an undisclosed expert.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 155 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Balogh, R., Byrne, M. Developing in the intertidal: effects of salinity and temperature on development to the pentameral juvenile seastar, Parvulastra exigua. Mar Biol 168, 99 (2021). https://doi.org/10.1007/s00227-021-03902-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-021-03902-2

Search

Navigation