Abstract
Cold polar marine species have very slow embryonic and larval development rates. Antarctic echinoids, bivalve molluscs and brooding gastropods develop up to 12 times slower than temperate and tropical species, departing from Arrhenius relationships and outside the normal Q 10 of 2–3 associated with 10 °C reductions in biochemical reaction rates. The slowing of development at temperatures around 0 °C has been reported previously to be much greater than for other parts of the global marine temperature range. Here we spawned and reared embryos and larvae of the Antarctic limpet Nacella polaris at 0.6 °C to the post-torsional veliger stage. Spawned eggs were 221 µm in diameter. Development rates were three times slower than any previously reported for patellogastropod limpets, with first division at 2.5 h post-fertilisation, the gastrula stage being reached after 55 h, hatching occurring after 70–75 h and the trochophore stage being reached after around 100 h. The marked slowing of development around 0 °C matches that previously reported for other polar taxa. This supports the hypothesis that there is a cold marine physiological transition to markedly slower physiological rates at temperatures near 0 °C. The transition is especially apparent here for development, but has also been reported for growth, both of which involve significant protein synthesis.


Similar content being viewed by others
References
Arrhenius SA (1889) Über die Dissociationswärme und den Einflusß der Temperatur auf den Dissociationsgrad der Elektrolyte. Z Physik Chem 4:96–116
Bashevkin SM, Pechenik JA (2015) The interactive influence of temperature and salinity on larval and juvenile growth in the gastropod Crepidula fornicata. J Exp Mar Biol Ecol 470:78–91
Bosch I, Beauchamp KA, Steele ME, Pearse JS (1987) Development, metamorphosis, and seasonal abundance of embryos and larvae of the Antarctic sea urchin Sterechinus neumayeri. Biol Bull 173:126–135
Bowden DA, Clarke A, Peck LS, Barnes DKA (2006) Antarctic sessile marine benthos: colonisation and growth on artificial substrata over 3 years. Mar Ecol Prog Ser 316:1–16
Buckland-Nicks J, Gibson G, Koss R (2002) Phylum mollusca: gastropoda. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 261–287
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 Annu Rev 49:1–42
Clark MS, Peck LS (2009) HSP70 heatshock proteins and environmental stress in Antarctic marine organisms: a mini-review. Mar Genomics 2:11–18
Clark MS, Fraser KPPF, Peck LS (2008) Lack of an HSP70 heat shock response in two Antarctic marine invertebrates. Polar Biol 31:1059–1065
Clarke A (1983) Life in cold water: the physiological ecology of polar marine ecotherms. Oceanogr Mar Biol Annu Rev 21:341–453
Clarke A (1992) Reproduction in the cold: thorson revisited. Invertbr Reprod Dev 22:175–184
Courtois De Viçose G, Viera MP, Bilbao A, Izquierdo MS (2007) Embryonic and larval development of Haliotis tuberculata coccinea Reeve: an indexed micro-photographic sequence. J Shellfish Res 26(3):847–854
Crofts DR (1937) The development of Haliotis tuberculata, with special reference to organogenesis during torsion. Phil Trans R Soc B 208:219–268
Damen P, Dictus WJAG (1994) Cell lineage of the prototroch of Patella vulgata (gastropoda, mollusca). Dev Biol 162:364–383
Fraser KPP, Clarke A, Peck LS (2007) Growth in the slow lane: protein metabolism in the Antarctic limpet Nacella concinna (Strebel, 1908). J Exp Biol 210:2691–2699
Graziano G (2014) On the mechanism of cold denaturation. Phys Chem Chem Phys 16:21755–21767
Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, Oxford
Hoegh-Guldberg O, Pearse JS (1995) Temperature, food availability and the development of marine invertebrate larvae. Am Zool 35:415–425
Hoffman JI, Peck LS, Hillyard G, Zieritz A, Clark MS (2010) No evidence for genetic differentiation between Antarctic limpet Nacella concinna morphotypes. Mar Biol 157:765–778
Hoffman JI, Clarke A, Linse K, Peck LS (2011) Effects of brooding and broadcasting reproductive modes on the population genetic structure of two Antarctic gastropod molluscs. Mar Biol 158:287–296
Hombron JB, Jacquinot CH (1841) Suite de la description de quelques mollusques, provenant de la campagne de l’Astrolabe et de la Zélée. Annales des Sciences Naturelles 2. Zoologie 16:190–192
Hyman LH (1992) The invertebrates: mollusca 1. International Books and Periodicals Supply, Delhi
Kay MC, Emlet RC (2002) Laboratory spawning, larval development, and metamorphosis of the limpets Lottia digitalis and Lottia asmi (Patellogastropoda, Lotiidae). Invertebr Biol 121:11–24
Kolbin KG (2006) Reproduction and development of the limpet Limalepeta lima (Dall, 1918) (Gastropoda: Lepetidae). Russ J Mar Biol 32:265–267
Kolbin KG, Kulikova VA (2011) Reproduction and larval development of the limpet Lottia persona (Rathke, 1833) (Gastropoda: Lottiidae) Russian J. Mar Biol 37:239–242
Koppen CL, Glascock JR, Holyoak AR (1996) Spawning and larval development of the ribbed limpet, Lottia digitalis (Rathke, 1833). Veliger 39:241–243
Lu JY, Chen ZS, Wu JY, Zeng H, Su GH (2001) Embryonic development of abalone (Haliotis diversicolor Reeve). Acta Zool Sin 47:317–323
Marshall DJ, Krug PJ, Kupriyanova EK, Byrne M, Emlet RB (2012) The biogeography of marine invertebrate life histories. Annu Rev Ecol Evol Syst 43:97–114
Pearse JS (1969) Slow developing demersal embryos and larvae of the Antarctic sea star Odontaster validus. Mar Biol 3:110–116
Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297
Pechenik JA, Tyrell AS (2015) Larval diet alters larval growth rates and post-metamorphic performance in the marine gastropod Crepidula fornicata. Mar Biol 162:1597–1610
Peck LS (1983) An investigation into the growth and early development of the ormer, Haliotis tuberculata (L.). Ph.D. thesis, CNAA, Portsmouth Polytechnic
Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40
Peck LS (2016) A cold limit to adaptation in the sea. Trends Ecol Evol 31(1):13–26
Peck LS, Clarke A, Chapman AL (2006a) Metabolism and development of pelagic larvae of Antarctic gastropods with mixed reproductive strategies. Mar Ecol Prog Ser 318:213–220
Peck LS, Convey P, Barnes DKA (2006b) Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol Rev 81:75–109
Peck LS, Powell DK, Tyler PA (2007) Very slow development in two Antarctic bivalve molluscs, the infaunal clam, Laternula elliptica and the scallop Adamussium colbecki. Mar Biol 150:1191–1197
Picken GB (1980) Distribution, growth, and reproduction of the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). J Exp Mar Biol Ecol 42:71–85
Picken GB, Allen D (1983) Unique spawning behaviour by the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908). J Exp Mar Biol Ecol 71(3):283–287
Place SP, Hofmann GE (2005) Constitutive expression of a stress-inducible heatshock protein gene, hsp70, in a phylogenetically distant Antarctic fish. Polar Biol 28:261–267
Powell AWB (1951) Antarctic and subantarctic mollusca: pelecypoda and gastropoda. Discov Rep (USA) 26:49–196
Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and ageing on fertilization success in the Antarctic clam Laternula elliptica and the Antarctic limpet Nacella concinna. Mar Ecol Prog Ser 215:191–200
Przeslawski R, Perino L, Padilla DK (2012) Effects of larval density and food rations on the larval development of an ecologically important bivalve (Mercenaria mercenaria). Molluscan Res 32:27–35
Schmidt-Nielsen K (1980) Animal physiology, 2nd edn. Cambridge University Press, Cambridge
Sharqawy MH, Lienhard VJH, Zubair SM (2010) The thermophysical properties of seawater: a review of existing correlations and data. Desalin Water Treat 16:354–380
Shin SC, Kim SJ, Lee JK, Ahn DH, Kim MG, Lee H et al (2012) Transcriptomics and comparative analysis of three Antarctic notothenioid fishes. PLoS One 7(8):e43762
Smith FGW (1935) The development of Patella vulgata. Phil Trans R Soc B 225:95–125
Somero GN (2004) Adaptation of enzymes to temperature: searching for basic ‘strategies’. Comp Biochem Physiol 139:321–333
Stanwell-Smith D, Clarke A (1998) The timing of reproduction in the Antarctic limpet Nacella concinna (Strebel, 1908) (Patellidae) at Signy island, in relation to environmental variables. J Molluscan Stud 64:123–127
Stanwell-Smith DP, Peck LS (1998) Temperature and embryonic development in relation to spawning and field occurrence of larvae of 3 Antarctic echinoderms. Biol Bull 194:44–52
Strebel H (1908) Dei gastropoden. Wissenschaftliche Ergebn. Schwedisch Sudpolar-Expedition 1901–1903(6):1–112
Vandenbiggelar JAM (1993) Cleavage pattern in embryos of Haliotis tuberculata (archaeogastropoda) and gastropod phylogeny. J Morphol 216:121–139
Vaugn D, Allen JD (2010) The peril of the plankton. Integr Comp Biol 50:552–570
Wägele JW (1987) On the reproductive biology of Ceratoserolis trilobitoides (Crustacea: Isopoda): latitudinal variation of fecundity and embryonic development. Polar Biol 7:11–24
Wong E, Davis AR, Byrne M (2010) Reproduction and early development in Haliotis coccoradiata (Vetigastropoda: Haliotidae). Invertbr Reprod Dev 54:77–87
Zimmerman KM, Pechenik JA (1989) How does temperature affect relative rates of growth and differentiation in the marine gastropod Crepidula plana. Am Zool 29:A174–A174
Acknowledgments
We thank the British Antarctic Survey dive team, and boatmen at Rothera station for support in animal collection and Ali Massey for assistance with laboratory equipment. We also thank Mairi Fenton for assistance in maintaining embryonic and larval cultures in 2012. The work was supported by core funding from the Natural Environment Research Council of the UK.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Peck, L.S., Heiser, S. & Clark, M.S. Very slow embryonic and larval development in the Antarctic limpet Nacella polaris . Polar Biol 39, 2273–2280 (2016). https://doi.org/10.1007/s00300-016-1894-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-016-1894-1


