Warming reduces metabolic rate in marine snails: Adaptation to fluctuating high temperatures challenges the metabolic theory of ecology

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1703, 2011, Pages 281-288

  Marshall, David J ^a   McQuaid, Christopher D ^b  

^a UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

^b RHODES UNIVERSITY   (South Africa)

Author keywords

Gastropod; Hypometabolism; Littorinidae; Metabolic rate depression; Thermal scaling

Indexed keywords

ACTIVATION ENERGY; ADAPTATION; EVOLUTIONARY BIOLOGY; HIGH TEMPERATURE; MARINE ECOSYSTEM; METABOLISM; REACTION KINETICS; ROCKY SHORE; SNAIL;

ANIMALIA; ECHINOLITTORINA; GASTROPODA; LITTORINIDAE;

EID: 78650496302     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1414     Document Type: Conference Paper

References (36)

1. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. 2001 Effects of size and temperature on metabolic rate. Science 293, 2248-2251. (doi:10.1126/science.1061967) (Pubitemid 32900233)
2. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. 2004 Toward a metabolic theory of ecology. Ecology 85, 1771-1789. (doi:10.1890/03-9000)
3. Gillooly, J. F., Allen, A. P., Savage, V. M., Charnov, E. L., West, G. B. & Brown, J. H. 2006 Response to Clarke and Fraser: effects of temperature on metabolic rate. Funct. Ecol. 20, 400-404. (doi:10.1111/j.1365-2435.2006. 01110.x) (Pubitemid 43725646)
4. Allen, A. P. & Gillooly, J. F. 2007 The mechanistic basis of the metabolic theory of ecology. Oikos 116, 1073-1077. (doi:10.1111/j.0030-1299. 2007.16079.x)
5. Clarke, A. 2004 Is there a universal temperature dependence of metabolism? Funct. Ecol. 8, 252-256.
6. Clarke, A. 2006 Temperature and the metabolic theory of ecology. Funct. Ecol. 20, 405-412. (doi:10.1111/j.1365-2435.2006.01109.x) (Pubitemid 43725647)
7. O'Connor, M. P., Kemp, S. J., Agosta, S. J., Hansen, F., Sieg, A. E., Wallace, B. P., McNair, J. N. & Dunham, A. E. 2007 Reconsidering the mechanistic basis of the metabolic theory of ecology. Oikos 116, 1058-1072. (doi:10.1111/j.0030-1299.2007.15534.x)
8. Hochachka, P. W. & Somero, G. N. 2002 Biochemical adaptation: mechanism and process in physiological evolution. Oxford, UK: Oxford University Press.
9. Clarke, A. & Fraser, K. P. P. 2004 Why does metabolism scale with temperature? Funct. Ecol. 18, 243-251. (doi:10.1111/j.0269-8463.2004.00841.x) (Pubitemid 38504288)
10. Irlich, U. M., Terblanche, J. S., Blackburn, T. M. &Chown, S. L. 2009 Insect rate-temperature relationships: environmental variation and the metabolic theory of ecology. Am. Nat. 174, 819-835. (doi:10.1086/647904)
11. Terblanche, J. S., Janion, C. & Chown, S. L. 2007 Variation in scorpion metabolic rate and rate-temperature relationships: implications for the fundamental equation of the metabolic theory of ecology. J. Evol. Biol. 20, 1602-1612. (doi:10.1111/j.1420-9101.2007.01322.x) (Pubitemid 46956634)
12. Marshall, D. J., McQuaid, C. D. & Williams, G. A. 2010 Non-climatic thermal adaptation: implications for species' responses to climate warming. Biol. Lett. (doi:10.1098/rsbl.2010.0233)
13. Gilchrist, G. W. 2000 The evolution of thermal sensitivity in changing environments. In Environmental stressors and gene response (eds K. B. Storey & J. Storey), pp. 55-69. Amsterdam, The Netherlands: Elsevier Science BV.
14. Angilletta, M. J., Wilson, R. S., Navas, C. A. & James, R. S. 2003 Tradeoffs and the evolution of thermal reaction norms. Trends Ecol. Evol. 18, 234-240. (doi:10.1016/S0169-5347(03)00087-9) (Pubitemid 36551228)
15. Guppy, M. & Withers, P. 1999 Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. 74, 1-40. (doi:10.1017/S0006323198005258) (Pubitemid 29215911)
16. Artacho, P. & Nespolo, R. F. 2009 Natural selection reduces energy metabolism in the garden snail, Helix aspera (Cornu aspersum). Evolution 63, 1044-1050. (doi:10.1111/j.1558-5646.2008.00603.x)
17. Newell, R. C. 1969 Effect of fluctuations in temperature on the metabolism of intertidal invertebrates. Am. Zool. 9, 293-307.
18. Percy, J. A. & Aldrich, F. A. 1971 Metabolic rate independent of temperature in mollusc tissue. Nature 231, 393-394. (doi:10.1038/231393a0)
19. Brown, A. C. & da Silva, F. M. 1984 Effects of temperature on oxygen consumption in two closely-related whelks from different temperature regimes. J. Exp. Mar. Biol. Ecol. 84, 145-153. (doi:10.1016/0022-0981(84)90207-7)
20. Marshall, D. J. & McQuaid, C. D. 1991 Metabolic rate depression in a marine pulmonate snail: pre-adaptation for a terrestrial existence? Oecologia 88, 274-276. (doi:10.1007/BF00320822)
21. Sokolova, I. M. & Pörtner, H. O. 2001 Physiological adaptations to high intertidal life involve improved water conservation abilities and metabolic rate depression in Littorina saxatilis. Mar. Ecol. Prog. Ser. 224, 71-86.
22. Hand, S. C. & Hardewig, I. 1996 Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu. Rev. Physiol. 58, 539-563. (doi:10.1146/annurev.ph.58.030196.002543)
23. Storey, K. B. & Storey, J. M. 2004 Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. 79, 207-233. (doi:10.1017/S1464793103006195) (Pubitemid 38282052)
24. Marshall, D. J. & McQuaid, C. D. 1992 Comparative aerial metabolism of the intertidal limpets Patella granularis L. (Mollusca: Prosobranchia) and Siphonaria oculus (Mollusca: Pulmonata). Physiol. Zool. 65, 1040-1056.
25. Houlihan, D. & Innes, A. J. 1982 Respiration in air and water of four Mediterranean trochids. J. Exp. Mar. Biol. Ecol. 57, 35-54. (doi:10.1016/0022-0981(82)90143-5)
26. Fretter, V. & Graham, A. 1976 A functional anatomy of invertebrates. New York, NY: Academic Press.
27. McMahon, R. F. 1990 Thermal tolerance, evaporative water loss, air-oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia 193, 241-260. (doi:10.1007/BF00028081)
28. Reid, D. G. 2007 The genus Echinolittorina (Habe, 1956) (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean. Zootaxa 1420, 1-161.
29. Sokolova, I. M. & Pörtner, H. O. 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. (doi:10.1242/jeb.00054) (Pubitemid 36108162)
30. McMahon, R. F., Russell-Hunter, W. D. & Aldridge, D. W. 1995 Lack ofmetabolic temperature compensation in the intertidal gastropods, Littorina saxatilis (Olivi) and L. obtusata (L.). Hydrobiologia 309, 89-100. (doi:10.1007/BF00014475)
31. Quinn, G. P. & Keough, M. J. 2002 Experimental design and data analysis for biologists. Cambridge, UK: Cambridge University Press.
32. Denny, M. W. & Harley, C. D. G. 2006 Hot limpets: predicting body temperatures in a conductance-mediated thermal system. J. Exp. Biol. 209, 2409-2419. (doi:10.1242/jeb.02257) (Pubitemid 44212831)
33. Bochdansky, A., Gronkjaer, P., Herra, T. & Leggett, W. 2005 Experimental evidence for selection against fish larva with high metabolic rate in a food limited environment. Mar. Biol. 47, 1413-1417.
34. Parsons, P. A. 2005 Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol. Rev. 80, 589-610. (doi:10.1017/S1464793105006822)
35. Helmuth, B., Kingsolver, J. G. & Carrington, E. 2005 Biophysics, physiological ecology, and climate change: does mechanism matter? Annu. Rev. Physiol. 67, 177-201. (doi:10.1146/annurev.physiol.67.040403.105027) (Pubitemid 40404490)
36. Gilman, S. E., Wethey, D. S. & Helmuth, B. 2006 Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales. Proc. Natl Acad. Sci. USA 103, 9560-9565. (doi:10.1073/pnas.0510992103) (Pubitemid 43955864)