Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism

Journal of Experimental Biology

Volumn 214, Issue 21, 2011, Pages 3649-3657

  Marshall, David J ^a   Dong, Yun Wei ^b   McQuaid, Christopher D ^c   Williams, Gray A ^d  

^a UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

^b XIAMEN UNIVERSITY   (China)

^c RHODES UNIVERSITY   (South Africa)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Gastropod; Hypometabolism; Littorinidae; Metabolic theory of ecology; Oxygen consumption

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ADAPTATION; ANIMAL; ARTICLE; BASAL METABOLIC RATE; BIOLOGICAL MODEL; BODY TEMPERATURE; BRUNEI DARUSSALAM; ENERGY METABOLISM; HEAT SHOCK RESPONSE; HONG KONG; LOCOMOTION; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; SNAIL; TEMPERATURE;

ADAPTATION, BIOLOGICAL; ADENOSINE TRIPHOSPHATE; ANIMALS; BASAL METABOLISM; BODY TEMPERATURE; BRUNEI; ENERGY METABOLISM; HEAT-SHOCK RESPONSE; HONG KONG; LOCOMOTION; MODELS, BIOLOGICAL; OXYGEN CONSUMPTION; SNAILS; TEMPERATURE;

ECHINOLITTORINA; GASTROPODA; LITTORINIDAE; METAZOA;

EID: 80054695847     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.059899     Document Type: Article

References (46)

1. Angilletta, M. J. (2009). Thermal Adaptation: A Theoretical And Empirical Synthesis. Oxford: Oxford University Press.
2. Angilletta, M. J., Wilson, R. S., Navas, C. A. and James, R. S. (2003). Tradeoffs and the evolution of thermal reaction norms. Trends Ecol. Evol. 18, 234-240. (Pubitemid 36551228)
3. Boutet, I., Tanguy, A., Le Guen, D., Piccino, P., Hourdez, S., Legendre, P. and Jollivet, D. (2009). Global depression in gene expression as a response to rapid thermal changes in vent mussels. Proc. R. Soc. B 276, 3071-3079.
4. Brown, A. C. and Da Silva, F. M. (1979). The effects of temperature on oxygen consumption in Bullia digitalis Meuschen (Gastropoda, Nassaridae). Comp. Biochem. Physiol. 62, 573-576. (Pubitemid 9146242)
5. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771-1789. (Pubitemid 39188101)
6. Cleland, J. D. and McMahon, R. F. (1986). Upper thermal limit of nine intertidal gastropod species from a Hong Kong rocky shore in relation to vertical distribution and desiccation associated with evaporative cooling. In Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong (ed. B. Morton), pp. 1141-1152. Hong Kong: Hong Kong University Press.
7. Dahlhoff, E. P. (2004). Biochemical indicators of stress and metabolism: Applications for marine ecological studies. Annu. Rev. Physiol. 66, 183-207. (Pubitemid 40614443)
8. Denny, M. W., Miller, L. P. and Harley, C. D. G. (2006). Thermal stress on intertidal limpets: Long-term hindcasts and lethal limits. J. Exp. Biol. 209, 2420-2431. (Pubitemid 44212832)
9. Dillon, M. E., Wang, G. and Huey, R. B. (2010). Global metabolic impacts of recent climate warming. Nature 467, 704-706.
10. Dong, Y. W., Miller, L. P., Sanders, J. and Somero, G. N. (2008). Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: Interspecific variation in constitutive and inducible synthesis reflects in situ exposure to heat stress. Biol. Bull. 215, 173-181.
11. Feder, M. E. and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243-282. (Pubitemid 29143171)
12. Garrabou, J., Coma, R., Bensoussan, N., Bally, M., Chevaldonné, P., Cigliano, M., Diaz, D., Harmenlini, J. G., Gambi, M. C., Kersting, D. K. et al. (2009). Mass mortality in Northwestern Mediterranean rocky benthic communities: Effects of the 2003 heat wave. Glob. Change Biol. 15, 1090-1103.
13. Garrity, S. D. (1984). Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 65, 559-574. (Pubitemid 16273248)
14. Gilchrist, G. W. (1995). Specialists and generalists in changing environments in fitness landscapes of thermal sensitivity. Am. Nat. 146, 252-270. (Pubitemid 26450753)
15. Gilchrist, G. W. (2000). The evolution of thermal sensitivity in changing environments. In Environmental Stressors and Gene Response (ed. K. B. Storey and J. M. Storey), pp. 55-69. Amsterdam: Elsevier Science.
16. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. and Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science 293, 2248-2251. (Pubitemid 32900233)
17. Guppy, M. and Withers, P. (1999). Metabolic depression in animals: Physiological perspectives and biochemical generalizations. Biol. Rev. Camb. Philos. Soc. 74, 1-40. (Pubitemid 29215911)
18. Harley, C. D. G. (2008). Tidal dynamics, topographic orientation, and temperaturemediated mass mortalities on rocky shores. Mar. Ecol. Prog. Ser. 371, 37-46.
19. Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford: Oxford University Press.
20. Hofmann, G. E. and Somero, G. N. (1996). Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol. Mar. Biol. Biotechnol. 5, 175-184.
21. Huey, R. B. and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4, 131-135.
22. Huey, R. B. and Stevenson, R. D. (1979). Integrating thermal physiology and ecology of ectotherms: Discussion of approaches. Am. Zool. 19, 357-366.
23. Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257. (Pubitemid 40404492)
24. Logan, C. A. and Somero, G. N. (2011). Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1373-R1383.
25. Marshall, D. J. and 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.
26. Marshall, D. J. and McQuaid, C. D. (2011). Warming reduces metabolic rate in marine snails: Adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proc. R. Soc. B 278, 281-288.
27. Marshall, D. J., McQuaid, C. D. and Williams, G. A. (2010). Non-climatic thermal adaptation: Implications for species' responses to climate warming. Biol. Lett. 6, 669-673.
28. McMahon, R. F. (1990). Thermal tolerance, evaporative water loss, air-oxygen consumption and zonation of intertidal prosobranchs: A new synthesis. Hydrobiologia 193, 241-260.
29. McMahon, R. F., Hunter, W. D. R. and Aldridge, D. W. (1995). Lack of metabolic temperature compensation in the intertidal gastropods, Littorina saxatilis (Olivi) and L. obtusata (L.). Hydrobiologia 309, 89-100.
30. Miller, L. P., Harley, C. D. G. and Denny, M. W. (2009). The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet, Lottia gigantea. Funct. Ecol. 23, 756-767.
31. Muñoz, J. L. P., Finke, G. R., Camus, P. A. and Bozinovic, F. (2005). Thermoregulatory behavior, heat gain and thermal tolerance in the periwinkle Echinolittorina peruviana in central Chile. Comp. Biochem. Physiol. 142A, 92-98. (Pubitemid 41265920)
32. Newell, R. C. (1969). Effect of fluctuations in temperature on the metabolism of intertidal invertebrates. Am. Zool. 9, 293-307.
33. Newell, R. C. and Branch, G. M. (1980). The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv. Mar. Biol. 17, 329-396.
34. Pörtner, H. O. (2002). Climate variations and the physiological basis of temperature dependent biogeography: Systemic to molecular hierarchy of thermal tolerance in animals. Comp. Biochem. Physiol. 132A, 739-761. (Pubitemid 34722582)
35. Pörtner, H. O. (2006). Climate-dependent evolution of Antarctic ectotherms: An integrative analysis. Deep Sea Res. II Top. Stud. Oceanogr. 53, 1071-1104. (Pubitemid 44177722)
36. Pörtner, H. O. (2010). Oxygen- and capacity-limitation of thermal tolerance: A matrix for integrating climate-related stressor effects in marine systems. J. Exp. Biol. 213, 881-893.
37. Pörtner, H. O. and Knust, R. (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95-97. (Pubitemid 46196986)
38. Reid, D. G. (2007). The genus Echinolittorina (Habe, 1956) (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean. Zootaxa 1420, 1-161. (Pubitemid 46501508)
39. Sokolova, I. M. and 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.
40. Sokolova, I. M. and 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. (Pubitemid 36108162)
41. Somero, G. N. (2002). Thermal physiology and vertical zonation of intertidal animals: Optima, limits, and costs of living. Integr. Comp. Biol. 42, 780-789. (Pubitemid 36224941)
42. Somero, G. N. (2005). Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits. Front. Zool. 2, 1.
43. Storey, K. B. and Storey, J. M. (2004). Metabolic rate depression in animals: Transcriptional and translational controls. Biol. Rev. 79, 207-233. (Pubitemid 38282052)
44. Tomanek, L. (2002). The heat-shock response: Its variation, regulation, and ecological importance in intertidal gastropods (genus Tegula). Integr. Comp. Biol. 42, 797-807. (Pubitemid 36224943)
45. Tomanek, L. and Somero, G. N. (1999). Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: Implications for limits of thermotolerance and biogeography. J. Exp. Biol. 202, 2925-2936.
46. Williams, G. A. and Morritt, D. (1995). Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar. Ecol. Prog. Ser. 124, 89-103. (Pubitemid 26452083)