What do metabolic rates tell us about thermal niches? Mechanisms driving crayfish distributions along an altitudinal gradient

Abstract

Humans are rapidly altering thermal landscapes, so a central challenge to organismal ecologists is to better understand the thermal niches of ectotherms. However, there is much disagreement over how we should go about this. Some ecologists assume that a statistical model of abundance as a function of habitat temperature provides a sufficient approximation of the thermal niche, but ecophysiologists have shown that the relationship between fitness and temperature can be complicated, and have stressed the need to elucidate the causal mechanisms underlying the response of species to thermal change. Towards this end, we studied the distribution of two crayfishes, Euastacus woiwuru and Euastacus armatus, along an altitudinal gradient, and for both species conducted experiments to determine the temperature-dependence of: (1) aerobic scope (the difference between maximum and basal metabolic rate; purported to be a proxy of the thermal niche); and (2) burst locomotor performance (primarily fuelled using anaerobic pathways). E. woiwuru occupied cooler habitats than E. armatus, but we found no difference in aerobic scope between these species. In contrast, locomotor performance curves differed significantly and strongly between species, with peak locomotor performances of E. woiwuru and E. armatus occurring at ~10 and ~18 °C, respectively. Crayfish from different thermal landscapes may have similar aerobic thermal performance curves but different anaerobic thermal performance curves. Our results support a growing body of literature implying different components of ectotherm fitness have different thermal performance curves, and further challenge our understanding of the ecology and evolution of thermal niches.

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References

  1. Addo-Bediako A, Chown SL, Gaston KJ (2002) Metabolic cold adaptation in insects: a large-scale perspective. Funct Ecol 16:332–338

    Article  Google Scholar 

  2. Angilletta MJ, Sears MW (2011) Coordinating theoretical and empirical efforts to understand the linkages between organisms and environments. Integr Comp Biol 51:653–661

    PubMed  Article  Google Scholar 

  3. Baldwin J, Gupta A, Iglesias X (1999) Scaling of anaerobic energy metabolism during tail flipping behaviour in the freshwater crayfish, Cherax destructor. Mar Freshwater Res 50:183–187

    Article  Google Scholar 

  4. Bernardo J, Spotila JR (2006) Physiological constraints on organismal response to global warming: mechanistic insights from clinally varying populations and implications for assessing endangerment. Biol Lett 2:135–139

    PubMed  PubMed Central  Article  Google Scholar 

  5. Brand MD (1990) The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J Theor Biol 145:267–286

    PubMed  Article  CAS  Google Scholar 

  6. Chown SL (2012) Trait-based approaches to conservation physiology: forecasting environmental change risks from the bottom up. Philos Trans R Soc B 367:1615–1627

    Article  Google Scholar 

  7. Clark TD, Jeffries KM, Hinch SG, Farrell AP (2011) Exceptional aerobic scope and cardiovascular performance of pink salmon (Oncorhynchus gorbuscha) may underlie resilience in a warming climate. J Exp Biol 214:3074–3081

    PubMed  Article  CAS  Google Scholar 

  8. Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782

    PubMed  Article  Google Scholar 

  9. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  10. Claussen DL (1980) Thermal acclimation in the crayfish Orconectes rusticus and O. virilis. Comp Biochem Physiol A Physiol 66:377–384

    Article  Google Scholar 

  11. Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am Nat 177:738–751

    PubMed  Article  Google Scholar 

  12. Cooke SJ et al (2013) What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol 1:1–23

    Article  Google Scholar 

  13. Deutsch CA et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672

    PubMed  PubMed Central  Article  Google Scholar 

  14. Ern R, Huong DTT, Phuong NT, Wang T, Bayley M (2014) Oxygen delivery does not limit thermal tolerance in a tropical eurythermal crustacean. J Exp Biol 217:809–814

    PubMed  Article  Google Scholar 

  15. Fangue NA, Richards JG, Schulte PM (2009) Do mitochondrial properties explain intraspecific variation in thermal tolerance? J Exp Biol 212:514–522

    PubMed  Article  CAS  Google Scholar 

  16. Grans A et al (2014) Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut. J Exp Biol 217:711–717

    PubMed  Article  CAS  Google Scholar 

  17. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40

    PubMed  Article  CAS  Google Scholar 

  18. Hare KM, Pledger S, Thompson MB, Miller JH, Daugherty CH (2010) Nocturnal lizards from a cool-temperate environment have high metabolic rates at low temperatures. J Comp Physiol B 180:1173–1181

    PubMed  Article  Google Scholar 

  19. Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85:107–119

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  21. Herberholz J, Sen MM, Edwards DH (2004) Escape behavior and escape circuit activation in juvenile crayfish during prey–predator interactions. J Exp Biol 207:1855–1863

    PubMed  Article  Google Scholar 

  22. Holt RD (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proc Natl Acad Sci USA 106:19659–19665

    PubMed  PubMed Central  Article  Google Scholar 

  23. Jimenez AG, Locke BR, Kinsey ST (2008) The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans. J Exp Biol 211:3214–3225

    PubMed  Article  CAS  Google Scholar 

  24. Johnston IA, Calvo J, Guderley H, Fernandez D, Palmer L (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    PubMed  CAS  Google Scholar 

  25. Kearney M, Porter W (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 12:334–350

    PubMed  Article  Google Scholar 

  26. Kearney M, Simpson SJ, Raubenheimer D, Helmuth B (2010) Modelling the ecological niche from functional traits. Philos Trans R Soc B 365:3469–3483

    Article  Google Scholar 

  27. Kingsolver JG (2009) The well-temperatured biologist. Am Nat 174:755–768

    PubMed  Article  Google Scholar 

  28. Kooijman SALM (2009) Dynamic energy budget theory for metabolic organisation. Cambridge University Press, Cambridge

    Google Scholar 

  29. Leibold MA (1995) The niche concept revisited: mechanistic models and community context. Ecology 76:1371–1382

    Article  Google Scholar 

  30. Lucassen M, Koschnick N, Eckerle LG, Portner HO (2006) Mitochondrial mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J Exp Biol 209:2462–2471

    PubMed  Article  CAS  Google Scholar 

  31. Magnuson JJ, Destasio BT (1996) Thermal niche of fishes and global warming. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish, 61st edn. Cambridge University Press, Cambridge, pp 377–408

    Google Scholar 

  32. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    PubMed  Article  Google Scholar 

  33. Nisbet RM, Muller EB, Lika K, Kooijman S (2000) From molecules to ecosystems through dynamic energy budget models. J Anim Ecol 69:913–926

    Article  Google Scholar 

  34. Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217:244–251

    PubMed  Article  Google Scholar 

  35. Pavey CR, Fielder DR (1996) The influence of size differential on agonistic behaviour in the freshwater crayfish, Cherax cuspidatas (Decapoda: Parastacidae). J Zool 238:445–457

    Article  Google Scholar 

  36. Portner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893

    PubMed  Article  Google Scholar 

  37. Portner HO, Schulte PM, Wood CM, Schiemer F (2010) Niche dimensions in fishes: an integrative view. Physiol Biochem Zool 83:808–826

    PubMed  Article  CAS  Google Scholar 

  38. Reidy SP, Nelson JA, Tang Y, Kerr SR (1995) Post-exercise metabolic rate in Atlantic cod and its dependence upon the method of exhaustion. J Fish Biol 47:377–386

    Article  Google Scholar 

  39. Rutledge PS, Pritchard AW (1981) Scope for activity in the crayfish, Pacifastacus leniusculus. Am J Physiol 240:R87–R92

    PubMed  CAS  Google Scholar 

  40. Sandblom E, Grans A, Axelsson M, Seth H (2014) Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future. Proc R Soc B 281:9

    Article  Google Scholar 

  41. Savage VM et al (2004) The predominance of quarter-power scaling in biology. Funct Ecol 18:257–282

    Article  Google Scholar 

  42. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702

    PubMed  Article  Google Scholar 

  43. Sears MW, Raskin E, Angilletta MJ (2011) The world is not flat: defining relevant thermal landscapes in the context of climate change. Integr Comp Biol 51:666–675

    PubMed  Article  Google Scholar 

  44. Seebacher F, Franklin CE (2012) Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology. Philos Trans R Soc B 367:1607–1614

    Article  Google Scholar 

  45. Seebacher F, Brand MD, Else PL, Guderley H, Hulbert AJ, Moyes CD (2010) Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol Biochem Zool 83:721–732

    PubMed  Article  CAS  Google Scholar 

  46. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920

    PubMed  Article  CAS  Google Scholar 

  47. Sommer AM, Portner HO (2004) Mitochondrial function in seasonal acclimatization versus latitudinal adaptation to cold in the lugworm Arenicola marina (L.). Physiol Biochem Zool 77:174–186

    PubMed  Article  CAS  Google Scholar 

  48. Soofiani NM, Priede IG (1985) Aerobic metabolic scope and swimming performance in juvenile cod, Gadus morhua L. J Fish Biol 26:127–138

    Article  Google Scholar 

  49. Steffensen JF (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59

    PubMed  Article  CAS  Google Scholar 

  50. Stoffels RJ (2015) Physiological trade-offs along a fast-slow lifestyle continuum in fishes: what do they tell us about resistance and resilience to hypoxia? PLoS One 10:e0130303

    PubMed  PubMed Central  Article  Google Scholar 

  51. Taniguchi Y, Nakano S (2000) Condition-specific competition: implications for the altitudinal distribution of stream fishes. Ecology 81:2027–2039

    Article  Google Scholar 

  52. Tracy CR, Christian KA (1986) Ecological relations among space, time, and thermal niche axes. Ecology 67:609–615

    Article  Google Scholar 

  53. West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592

    PubMed  Article  Google Scholar 

  54. White CR, Seymour RS (2011) Physiological functions that scale to body mass in fish. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Elsevier, Amsterdam, pp 1573–1582

    Google Scholar 

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Acknowledgments

We thank John Morrongiello and Slade Allen-Ankins for their reviews of earlier drafts. Leon Barmuta and an anonymous reviewer provided extensive feedback that improved the paper. We thank Kyle Weatherman, Glenn Miller and Rachel Press for assistance in the lab. Susan Lawler provided great insight on the natural history of Euastacus. This work was carried out under VIC Fisheries Permits 2010-23NC and National Parks Permit 10005630. This work was partly funded by the CSIRO Land and Water Flagship, the Murray-Darling Freshwater Research Centre and the Goulburn-Broken Catchment Management Authority.

Author contribution statement

R. J. S. conceived and designed the study. A. J. R., M. T. V., S. P. C. and R. J. S. carried out field surveys, temperature logging and experiments. W. J. M. and R. J. S. analysed the data. R. J. S. wrote the paper; other authors provided editorial advice.

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Correspondence to Rick J. Stoffels.

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All applicable institutional and/or national guidelines for the care and use of animals were followed. This work was carried out under La Trobe University Ethics permits AEC-09-50W, AEC-12-07, and AEC-10-55.

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Communicated by Leon A. Barmuta.

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Stoffels, R.J., Richardson, A.J., Vogel, M.T. et al. What do metabolic rates tell us about thermal niches? Mechanisms driving crayfish distributions along an altitudinal gradient. Oecologia 180, 45–54 (2016). https://doi.org/10.1007/s00442-015-3463-7

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Keywords

  • Climate change
  • Community ecology
  • Functional traits
  • Metabolic ecology
  • Trade-off