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Long-term acclimation and potential scope for thermal resilience in Southern Ocean bivalves

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Abstract

Different physiological thresholds of species across biogeographic boundaries can show a long-term scope for adaptation. Characterised by cold-stenothermal conditions, polar and deep-sea environments are constrained by thermal stability across wide regions, and polar invertebrates are broadly considered to be highly sensitive to only subtle changes in thermal regime. We examine the respiratory response of two distinct biogeographic populations of the widespread bivalve Lissarca notorcadensis from deep waters in the Southern Ocean to acute thermal changes, and present distinct respiratory responses for each population. Populations from the Weddell Sea living in cooler water temperatures (<0 °C) show a lower tolerance to temperature increases, identified by an increase in oxygen consumption at temperatures from −1 to 4 °C and mortality at 5 °C. In contrast, populations from the Scotia Sea, experiencing a thermally more variable cold-stenothermal environment driven by seasonality, show no significant increase in oxygen consumption up to 6 °C before peaking at 8 °C, and mortality during acclimation to 9 °C. Our results are discussed in relation to the hypothesis that long-term adaptation to thermal envelopes, over multiple generations, likely determines the degree of thermal resilience to warming and at population-specific levels. This contrasts to previous laboratory-based (short-term acclimation or acute) thermal response studies, which have shown high sensitivities and low acclimation capacities to temperature increases. We highlight the need for long-term acclimation studies and pose questions as to how selection for population-specific thermal tolerances may take place in a global warming scenario and within a macroecological context.

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References

  • Aronson RB, Thatje S, Clarke A, Peck LS, Blake DB, Wilga CD, Seibel BA (2007) Climate change and invasibility of the Antarctic Benthos. Annu Rev Ecol Evolut Syst 38:129–154

    Article  Google Scholar 

  • Aronson RB, Thatje S, McClintock JB, Hughes K (2011) Anthropogenic impacts on marine ecosystems in Antarctica. Ann Rev NY Acad Sci 1223:82–107

    Article  Google Scholar 

  • Barnes DKA, Fuentes V, Clarke A, Schloss IR, Wallace MI (2006) Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep Sea Res II 53:853–865

    Article  Google Scholar 

  • Benson BB, Krause D (1984) The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnol Oceanogr 29:620–637

    Article  CAS  Google Scholar 

  • Bilyk KT, DeVries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A 158:382–390

    Article  Google Scholar 

  • Brey T, Hain S (1992) Growth, reproduction and production of Lissarca notorcadensis (Bivalvia: Philobryidae) in the Weddell Sea, Antarctica. Mar Ecol Prog Ser 82:219–226

    Article  Google Scholar 

  • Brey T, Starmans A, Magiera U, Hain S (1993) Lissarca notorcadensis (Bivalvia: Philobryidae) living on Notocidaris sp. (Echinoida: Cidaridae): population dynamics in limited space. Polar Biol 13:89–95

    Article  Google Scholar 

  • Brey T, Voigt M, Jenkins K, Ahn IY (2011) The bivalve Laternula elliptica at King George Island—a biological recorder of climate forcing in the West Antarctic Peninsula region. J Mar Syst 88:542–552

    Article  Google Scholar 

  • Carmack EC, Foster TD (1975) On the flow of water out of the Weddell Sea. Deep Sea Res 22:711–724

    Google Scholar 

  • Clarke A, Crame JA (1989) The origin of the Southern Ocean marine fauna. In: Crame JA (ed) Origins and evolution of the Antarctic Biota. vol 47. Geological Society Special Publication, London, UK, pp 253–268

  • Clarke A, Gore DJ (1992) Egg size and composition in Ceratoserolis (Crustacea: Isopoda) from the Weddell Sea. Polar Biol 12:129–134

    Article  Google Scholar 

  • Cope T, Linse K (2006) Morphological differences in Lissarca notorcadensis Melvill and Standen, 1907 from the Scotia, Weddell and Ross Seas. Deep Sea Res II 53:903–911

    Article  Google Scholar 

  • Dell RK (1990) Antarctic Mollusca with special reference to the fauna of the Ross Sea. Bull R Soc NZ 27:1–311

    Google Scholar 

  • Eastman JT, Devries AL (1997) Biology and phenotypic plasticity of the Antarctic nototheniid fish Trematomus newnesi in McMurdo Sound. Antarct Sci 9:27–35

    Article  Google Scholar 

  • Fahrbach E, Rohardt G, Scheele N, Schröder M, Strass V, Wisotzki A (1995) Formation and discharge of deep and bottom water in the north western Weddell Sea. J Mar Res 53:515–538

    Article  Google Scholar 

  • Fangue NA, Hofmeister Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872

    Article  CAS  Google Scholar 

  • Fraser WR, Hofmann EE (2003) A predator’s perspective on causal links between climate change, physical forcing and ecosystem response. Mar Ecol Prog Ser 265:1–15

    Article  Google Scholar 

  • Hall S, Thatje S (2011) Temperature-driven biogeography of the deep-sea family Lithodidae (Crustacea: Decapoda: Anomura) in the Southern Ocean. Polar Biol 34:363–370

    Article  Google Scholar 

  • Harper EM, Clark MS, Hoffman JI, Philipp EER, Peck LS (2012) Iceberg scour and shell damage in the Antarctic bivalve Laternula elliptica. PLoS ONE 7:e46341

    Article  CAS  Google Scholar 

  • Hoffmann AA (2010) Physiological climatic limits in Drosophila: patterns and implications. J Exp Biol 213:870–880

    Article  CAS  Google Scholar 

  • Kuo ESL, 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 

  • Linse K, Barnes DKA, Enderlein P (2006) Body size and growth of benthic invertebrates along an Antarctic latitudinal gradient. Deep Sea Res II 53:921–931

    Article  Google Scholar 

  • Linse K, Cope T, Lörz AN, Sands C (2007) Is the Scotia Sea a centre of Antarctic marine diversification? Some evidence of cryptic speciation in the circum-Antarctic bivalve Lissarca notorcadensis (Arcoidea: Philobryidae). Polar Biol 30:1059–1068

    Article  Google Scholar 

  • Locarnini RA, Mishonov AV, Antonov JI, Boyer TP, Garcia HE, Baranova OK, Zweng MM, Paver CR, Reagan JR, Johnson DR, Hamilton M, Seidov D (2013) World ocean atlas 2013, vol 1. Temperature. In: Levitus S, Ed., Mishonov A Technical Ed. NOAA Atlas NESDIS 73

  • Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604

    Article  Google Scholar 

  • Meredith MP, Brown PJ, Garabato CAN, Jullion L, Venables HJ, Messias MJ (2013) Dense waters of the Weddell Sea and Scotia Seas: recent changes in properties and circulation. Philos Trans R Soc A 372:1–11

    Google Scholar 

  • Morley SA, Hirse T, Pörtner HO, Peck LS (2009) Geographic variation in thermal tolerance within Southern Ocean marine ectotherms. Comp Biochem Physiol A 153:154–161

    Article  Google Scholar 

  • Morley SA, Lemmon V, Obermüller Spicer JI, Clark MS, Peck LS (2011) Duration tenacity: a method for assessing acclimatory capacity of the Antarctic limpet, Nacella concinna. J Exp Mar Biol Ecol 399:39–42

    Article  Google Scholar 

  • Morley SA, Belchier M, Sands C, Barnes DKA, Peck LS (2014) Geographic isolation and physiological mechanisms underpinning species distributions at the range limit hotspot of South Georgia. Rev Fish Biol Fisheries 24:485–492

    Article  Google Scholar 

  • Oliphant A, Thatje S, Brown A, Morini M, Ravaux J, Shillito B (2011) Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window. J Exp Biol 214:1109–1117

    Article  Google Scholar 

  • Peck LS, Pörtner HO, Hardewig I (2002) Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula elliptica. Physiol Biochem Zool 75:123–133

    Article  Google Scholar 

  • Peck LS, Webb KE, Bailey DM (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630

    Article  Google Scholar 

  • Peck LS, Webb KE, Miller A, Clark MS, Hill T (2008) Temperature limits to activity, feeding and metabolism in the Antarctic starfish Odantaster validus. Mar Ecol Prog Ser 358:181–189

    Article  Google Scholar 

  • Peck LS, Massey A, Thorne MAS, Clark MS (2009) Lack of acclimation in Ophionotus victoriae: brittle stars are not fish. Polar Biol 32:399–402

    Article  Google Scholar 

  • Peck LS, Morley SA, Clark MS (2010) Poor acclimation capacities in Antarctic marine ectotherms. Mar Biol 157:2051–2059

    Article  Google Scholar 

  • Peck LS, Morley SA, Richard J, Clark MS (2014) Acclimation and thermal tolerance in Antarctic marine ectotherms. J Exp Biol 217:16–22

    Article  Google Scholar 

  • Piacentino GLM, Barro-Oro E (2009) Phenotypic plasticity in the Antarctic fish Trematomus newnesi (Nototheniidae) from the South Shetland Islands. Polar Biol 32:1407–1413

    Article  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692

    Article  Google Scholar 

  • Pörtner HO, Hardewig I, Peck LS (1999) Mitochondrial function and critical temperature in the Antarctic bivalve, Laternula elliptica. Comp Biochem Physiol A 124:179–189

    Article  Google Scholar 

  • Prezant RS, Showers M, Winstead RL, Cleveland C (1992) Reproductive ecology of the Antarctic bivalve Lissarca notorcadensis (Philobryidae). Am Malac Bull 9:173–186

    Google Scholar 

  • Ravaux J, Léger N, Rabet N, Morini M, Zbinden M, Thatje S, Shillito B (2012) Adaptation to thermally variable environments: capacity for acclimation of thermal limit and heat shock response in the shrimp Palaemonetes varians. J Comp Physiol B 182:899–907

    Article  CAS  Google Scholar 

  • Reed AJ, Thatje S, Linse K (2012) Shifting baselines in Antarctic ecosystems; ecophysiological response to warming in Lissarca miliaris at Signy Island, Antarctica. PLoS ONE 7:e53477

    Article  CAS  Google Scholar 

  • Reed AJ, Morris JP, Linse K, Thatje S (2013) Plasticity in shell morphology and growth among deep-sea protobranch bivalves of the genus Yoldiella (Yoldiidae) from contrasting Southern Ocean regions. Deep Sea Res I 81:14–24

    Article  Google Scholar 

  • Reed AJ, Linse K, Thatje S (2014) Differential adaptations between cold-stenothermal environments in the bivalve Lissarca cf. miliaris (Philobryidae) from the Scotia Sea islands and Antarctic Peninsula. J Sea Res 88:11–20

    Article  Google Scholar 

  • Richard J, Morley SA, Thorne MAS, Peck LS (2012) Estimating long-term survival temperatures at the assemblage level in the marine environment: towards macrophysiology. PLoS ONE 7:e34655

    Article  CAS  Google Scholar 

  • Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Saucède T, Griffiths H, Moreau C, Jackson JA, Sands C, Downey R, Reed A, Mackenzie M, Geissler P, Linse K (2015) East Weddell Sea echinoids from the JR275 expedition. ZooKeys 504:1–10

    Article  Google Scholar 

  • Schofield O, Ducklow HW, Martinson DG, Meredith MP, Moline MA, Fraser WR (2010) How do polar marine ecosystems respond to rapid climate change? Science 328:1520–1523

    Article  CAS  Google Scholar 

  • Smith DA, Hofmann EE, Klinck JM, Lasarca CM (1999) Hydrography and circulation of the West Antarctic Peninsula continental shelf. Deep Sea Res I 46:925–949

    Article  Google Scholar 

  • Sokolova IM, Pörtner HO (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207

    Article  Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65

    Article  CAS  Google Scholar 

  • Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of Eastern Pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73:200–208

    Article  CAS  Google Scholar 

  • Thatje S (2012) Effects of capability for dispersal on the evolution of diversity in Antarctic benthos. Integr Comp Biol 52:470–482

    Article  Google Scholar 

  • Thatje S, Hillenbrand CD, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540

    Article  Google Scholar 

  • Thatje S, Hillenbrand CD, Mackensen A, Larter R (2008) Life hung by a thread: endurance of Antarctic fauna in glacial periods. Ecology 89(3):682–692

    Article  Google Scholar 

  • Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294

    Article  Google Scholar 

  • Wägele JW (1987) On the reproductive biology of Ceratoserolis trilobitoides (Crustacea: Isopoda): Latitudinal variation in fecundity and embryonic development. Polar Biol 7:11–24

    Article  Google Scholar 

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Acknowledgments

We thank Captain Burgan and his crew of RRS James Clark Ross as well as PSOs Phil Leat and Huw Griffiths and their teams for help and support on board. We thank Katrin Linse (British Antarctic Survey) for her comments on an earlier version of this manuscript. The authors would also like to thank the two reviewers and Patrick Gagnon for constructive comments that helped improve the manuscript. AJR was supported through a Natural Environment Research Council PhD studentship. AJR’s participation in JR275 was supported through a Collaborative Gearing Scheme Grant.

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Correspondence to Adam J. Reed.

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Reed, A.J., Thatje, S. Long-term acclimation and potential scope for thermal resilience in Southern Ocean bivalves. Mar Biol 162, 2217–2224 (2015). https://doi.org/10.1007/s00227-015-2752-3

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