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Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica

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Abstract

Animal responses to changing environments are most commonly studied in relation to temperature change. The current paradigm for marine ectotherms is that temperature limits are set through oxygen limitation. Oxygen limitation leads to progressive reductions in capacity to perform work or activity, and these are more important and proximate measures of a population’s ability to survive. Here we measured the ability of a large Antarctic clam to rebury when removed from sediment at temperatures between −1.5 and 7.5 °C and at three oxygen concentrations, 10.2, 20.5 and 27.7%. The proportion of the population capable of reburying declined rapidly and linearly with temperature from around 65% at 0 °C to 0% at 6 °C in normoxia (20.5% O2). Decreasing oxygen to 10.2% reduced temperature limits for successful burial by around 2 °C, and increasing oxygen to 27.7% raised the limits by 1–1.5 °C. There was an interactive effect of body size and temperature on burying: the temperature limits of larger individuals were lower than smaller animals. Similarly, these size limits were increased by increasing oxygen availability. Considering data for all temperatures and oxygen levels, the fastest burying rates occurred at 3 °C, which is 2 °C above the maximum summer temperature at this site.

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References

  • Atkinson D, Morley SA, Hughes RN (2006) From cells to colonies: at what levels of body organisation does the “temperature size rule” apply? Evol Dev 8:202–214

    Google Scholar 

  • Bayne BL (1976) Marine mussels: their ecology and physiology. Cambridge University Press, Cambridge, p 506

    Google Scholar 

  • Brokordt KB, Himmelman JH, Guderley HE (2000) Effect of reproduction on escape responses and muscle metabolic capacities in the scallop Chlamys islandica Muller 1776. J Exp Mar Bio Ecol 251(2):205–225

    Article  PubMed  Google Scholar 

  • Cardillo M (2003) Biological determinants of extinction risk: why are smaller species less vulnerable? Anim Conserv 6:63–69

    Article  Google Scholar 

  • Chapelle G, Peck LS (1999) Polar gigantism dictated by oxygen availability. Nature 399:114–115

    Article  CAS  Google Scholar 

  • Chapelle G, Peck LS (2004) Amphipod crustacean size spectra: new insights in the relationship between size and oxygen. Oikos 106:167–175

    Article  Google Scholar 

  • Clarke A, Johnston N (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol Annu Rev 41:47–114

    Google Scholar 

  • Clarke A, Peck LS (1991) The physiology of polar marine zooplankton. Polar Res 10:355–369

    Article  Google Scholar 

  • Convey P, Pugh PJA, Jackson C, Murray AW, Ruhland CT, Xiong FS, Day TA (2002) Response of Antarctic terrestrial arthropods to long-term climate manipulations. Ecology 83:3130–3140

    Google Scholar 

  • Davenport J, Davenport JL (2006) Interaction of thermal tolerance and oxygen availability in the eurythermal gastropods Littorina littorea and Nucella lapillus. Mar Ecol Prog Ser 332:167–170

    Article  Google Scholar 

  • Davis AJ, Jenkinson LS, Lawton JH, Shorrocks B, Wood S (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature 391:783–786

    Article  PubMed  CAS  Google Scholar 

  • Fagan WF, Meir E, Prendergast J, Folarin A, Karieva P (2001) Characterising population vulnerability for 758 species. Ecol Lett 4:132–138

    Article  Google Scholar 

  • Frazier MR, Woods HA, Harrison JF (2001) Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiol Biochem Zool 74:641–650

    Article  PubMed  CAS  Google Scholar 

  • Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab Maja squinado. Am J Physiol Regul Integr Comp Physiol 279:R1531–R1538

    PubMed  CAS  Google Scholar 

  • Grassle JF, Maciolek NJ (1992) Deep sea species richness: regional and local diversity estimates from quantitative bottom samples. Am Nat 139:313–341

    Article  Google Scholar 

  • Jensen MN (2003) Consensus on ecological impact remains elusive. Science 299:38

    Article  PubMed  CAS  Google Scholar 

  • McClain CR, Rex MA (2001) The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Mar Biol 139:681–685

    Article  Google Scholar 

  • McKinney ML (1997) Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu Rev Ecol Syst 28:495–516

    Article  Google Scholar 

  • Mitchell JFB, Lowe J, Wood RA, Vellinga M (2006) Extreme events due to human-induced climate change. Philos Trans R Soc Lond A 364(1845):2117–2133

    Article  Google Scholar 

  • O’Grady JJ, Reed DH, Brook BW, Frankham R (2004) What are the best correlates of predicted extinction risk? Biol Conserv 118:513–520

    Article  Google Scholar 

  • Peck LS (1998) Feeding, metabolism and metabolic scope in Antarctic ectotherms. In: Pörtner HO, Playle R (eds) Cold ocean physiology, vol 66 (Society for Experimental Biology Seminar Series). Cambridge University Press, Cambridge, pp 365–389

  • Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40

    Article  Google Scholar 

  • Peck LS (2005a) Prospects for survival in the Southern ocean: extreme temperature sensitivity of benthic species. R Soc Spec Issue Antarct Sci 17(4):497–507

    Google Scholar 

  • Peck LS (2005b) Prospects for surviving climate change in Antarctic aquatic species. Front Zool 2:9. DOI: 10.1186/1742-9994-2-9

  • Peck LS, Chapelle G (2003) Reduced oxygen at high altitude limits maximum size. Proc R Soc Lond B 270:S166–S167

    Google Scholar 

  • Peck LS, Conway LZ (2000) The myth of metabolic cold adaptation: oxygen consumption in stenothermal Antarctic bivalves. In: Harper EM, Taylor JD, Crame JA (eds) The evolutionary biology of the bivalvia. Geol Soc Spec Publ London 177:441–45

  • Peck LS, Maddrell SHP (2005) The limitation of size by oxygen in the fruit fly Drosophila melanogaster. J Exp Zool 303A:968–975

    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  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Peck LS, Ansell AD, Webb KE, Hepburn L, Burrows M (2004b) Movements and burrowing activity in the Antarctic bivalve molluscs Laternula elliptica and Yoldia eightsi. Polar Biol 27:357–367

  • Peck LS, Convey P, Barnes DKA (2006a) Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biol Rev 81:75–109

    Article  PubMed  Google Scholar 

  • Peck LS, Powell DK, Tyler PA (2006b) Very slow development in two Antarctic bivalve molluscs, the infaunal clam, Laternula elliptica and the scallop Adamussium colbecki. Mar Biol. DOI: 10.1007/s00227-006-0428-8

  • Pfitzenmeyer HT, Drobeck KG (1967) Some factors influencing reburrowing activity of soft-shell clam, Mya arenaria. Chesapeake Sci 8:193–199

    Article  Google Scholar 

  • Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  PubMed  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761

    Google Scholar 

  • Pörtner HO (2004) Climate variability and the energetic pathways of evolution: the origin of endothermy in mammals and birds. Physiol Biochem Zool 77:959–981

    Article  PubMed  Google Scholar 

  • Pörtner HO (2006) Climate dependent evolution of Antarctic ectotherms: an integrative analysis. Deep Sea Res II 53:1071–1104

    Article  Google Scholar 

  • Pörtner HO, Hardewig I, Sartorius FJ, van Dijk P (1998) Energetic aspects of cold adaptation: critical temperatures in metabolic, ionic and acid base regulation? In: Pörtner HO, Playle R (eds) Cold ocean physiology, vol 66 (Society for Experimental Biology Seminar Series). Cambridge University Press, Cambridge, pp 88–120

  • Pörtner HO, Peck LS, Zielinski S, Conway LZ (1999) Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature. Polar Biol 22:17–30

    Article  Google Scholar 

  • Pörtner HO, Peck LS, Hirse T (2006) Hyperoxia alleviates thermal stress in the Antarctic bivalve Laternula elliprica: evidence for oxygen limited thermal tolerance. Polar Biol 29:688–693

    Article  Google Scholar 

  • Powell DK (2001) The reproductive ecology of Antarctic free-spawning molluscs. Ph.D. Thesis, University of Southampton, Southampton, UK, p 142

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  PubMed  CAS  Google Scholar 

  • Soetaert K, Muthumbi A, Heip C (2002) Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns. Mar Ecol Prog Ser 242:179–193

    Article  Google Scholar 

  • Snelgrove PVR, Smith CR (2002) A riot of species in an environmental calm: the paradox of the species-rich deep-sea floor. Oceanogr Mar Biol Annu Rev 40:311–342

    Google Scholar 

  • Somero GN (2005) Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits. Front Zool 2:1. DOI: 10.1186/1742–9994-2-1

  • Somero GN, DeVries AL (1967) Temperature tolerance of some Antarctic fishes. Science 156:257–258

    Article  PubMed  CAS  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  PubMed  CAS  Google Scholar 

  • Weibel ER, Bacigalupe LD, Schmitt B, Hoppeler H (2004) Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir Physiol Neurobiol 140:115–132

    Article  PubMed  Google Scholar 

  • Woods HA, Hill RI (2004) Temperature-dependent oxygen limitation in insect eggs. J Exp Biol 207:2267–2276

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the divers and marine support team at Rothera research station, especially Matt Brown and Paul Mann. It benefited from diving support from the NERC Centre at Oban. This work is part of the BIOFLAME programme of science of the NERC British Antarctic Survey.

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Correspondence to Lloyd Samuel Peck.

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Communicated by Martin Attrill.

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Peck, L.S., Morley, S.A., Pörtner, HO. et al. Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica . Oecologia 154, 479–484 (2007). https://doi.org/10.1007/s00442-007-0858-0

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  • DOI: https://doi.org/10.1007/s00442-007-0858-0

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