Metabolism and energy supply below the critical thermal minimum of a chill-susceptible insect

Journal of Experimental Biology

Volumn 215, Issue 8, 2012, Pages 1366-1372

  MacMillan, Heath A ^a   Williams, Caroline M ^a   Staples, James F ^a   Sinclair, Brent J ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Chill susceptible; Chill coma; Critical thermal minimum; Oxygen and capacity limitation of thermal tolerance; Thermal limit; Thermolimit respirometry

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; CARBON DIOXIDE; LACTIC ACID;

ANIMAL; ARTICLE; BREATHING; COLD; ENERGY METABOLISM; FEMALE; FEMUR; GRYLLIDAE; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ALANINE; ANIMALS; CARBON DIOXIDE; COLD TEMPERATURE; ENERGY METABOLISM; FEMALE; FEMUR; GRYLLIDAE; LACTIC ACID; RESPIRATION;

EID: 84860116428     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.066381     Document Type: Article

References (52)

1. Addo-Bediako, A., Chown, S. L. and Gaston, K. J. (2000). Thermal tolerance, climatic variability and latitude. Proc. R. Soc. Lond. B 267, 739-745.
2. Chown, S. L., Jumbam, K. R., Sørensen, J. G. and Terblanche, J. S. (2009). Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct. Ecol. 23, 133-140.
3. Chown, S. L., Hoffmann, A. A., Kristensen, T. N., Angilletta, M. J., Jr, Stenseth, N. C. and Pertoldi, C. (2010). Adapting to climate change: a perspective from evolutionary physiology. Clim. Res. 43, 3-15.
4. Colinet, H. (2011). Disruption of ATP homeostasis during chronic cold stress and recovery in the chill susceptible beetle (Alphitobius diaperinus). Comp. Biochem. Physiol. 160A, 63-67.
5. Eliason, E. J., Clark, T. D., Hague, M. J., Hanson, L. M., Gallagher, Z. S., Jeffries, K. M., Gale, M. K., Patterson, D. A., Hinch, S. G. and Farrell, A. P. (2011). Differences in thermal tolerance among sockeye salmon populations. Science 332, 109-112.
6. Farrell, A. P., Hinch, S. G., Cooke, S. J., Patterson, D. A., Crossin, G. T., Lapointe, M. and Mathes, M. T. (2008). Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiol. Biochem. Zool. 81, 697-708.
7. Feala, J. D., Coquin, L., McCulloch, A. D. and Paternostro, G. (2007). Flexibility in energy metabolism supports hypoxia tolerance in Drosophila flight muscle: metabolomic and computational systems analysis. Mol. Syst. Biol. 3, 99.
8. Frederich, M. and Pörtner, H. O. (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.
9. Hamada, F. N., Rosenzweig, M., Kang, K., Pulver, S. R., Ghezzi, A., Jegla, T. J. and Garrity, P. A. (2008). An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217-220.
10. Harrison, J., Camazine, S., Marden, J. H., Kirkton, S. D., Rozo, A. and Yang, X. L. (2001). Mite not make it home: tracheal mites reduce the safety margin for oxygen delivery of flying honeybees. J. Exp. Biol. 204, 805-814.
11. Hazell, S. P. and Bale, J. S. (2011). Low temperature thresholds: are chill coma and CTmin synonymous? J. Insect Physiol. 57, 1085-1089.
12. Hoback, W. W. and Stanley, D. W. (2001). Insects in hypoxia. J. Insect Physiol. 47, 533-542.
13. Hoback, W. W., Podrabsky, J. E., Higley, L. G., Stanley, D. W. and Hand, S. C. (2000). Anoxia tolerance of con-familial tiger beetle larvae is associated with differences in energy flow and anaerobiosis. J. Comp. Physiol. B 170, 307-314.
14. Hosler, J. S., Burns, J. E. and Esch, H. E. (2000). Flight muscle resting potential and species-specific differences in chill-coma. J. Insect Physiol. 46, 621-627.
15. Judge, K. A. (2010). Female social experience affects the shape of sexual selection on males. Evol. Ecol. Res. 12, 389-402.
16. Klok, C. J. and Chown, S. L. (2003). Resistance to temperature extremes in sub-Antarctic weevils: interspecific variation, population differentiation and acclimation. Biol. J. Linn. Soc. 78, 401-414.
17. Klok, C. J., Sinclair, B. J. and Chown, S. L. (2004). Upper thermal tolerance and oxygen limitation in terrestrial arthropods. J. Exp. Biol. 207, 2361-2370.
18. Ko tál, V. and Tollarová-Borovanská, M. (2009). The 70 kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLoS ONE 4, e4546.
19. Ko tál, V., Vambera, J. and Bastl, J. (2004). On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J. Exp. Biol. 207, 1509-1521.
20. Ko tál, V., Yanagimoto, M. and Bastl, J. (2006). Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comp. Biochem. Physiol. 143B, 171-179.
21. Kovac, H., Stabentheiner, A., Hetz, S. K., Petz, M. and Crailsheim, K. (2007). Respiration of resting honeybees. J. Insect Physiol. 53, 1250-1261.
22. Lannig, G., Bock, C., Sartoris, F. J. and Pörtner, H. O. (2004). Oxygen limitation of thermal tolerance in cod, Gadus morhua L., studied by magnetic resonance imaging and on-line venous oxygen monitoring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R902-R910.
23. Lannig, G., Cherkasov, A. S., Pörtner, H. O., Bock, C. and Sokolova, I. M. (2008). Cadmium-dependent oxygen limitation affects temperature tolerance in eastern oysters (Crassostrea virginica Gmelin). Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1338-R1346.
24. Lighton, J. R. B. and Lovegrove, B. G. (1990). A temperature-induced switch from diffusive to convective ventilation in the honeybee. J. Exp. Biol. 154, 509-516.
25. Lighton, J. R. B. and Schilman, P. E. (2007). Oxygen reperfusion damage in an insect. PLoS ONE 2, e1267.
26. Lighton, J. R. B. and Turner, R. J. (2004). Thermolimit respirometry: an objective assessment of critical thermal maxima in two sympatric desert harvester ants, Pogonomyrmex rugosus and P. californicus. J. Exp. Biol. 207, 1903-1913.
27. MacMillan, H. A. and Sinclair, B. J. (2011a). The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the fall field cricket (Gryllus pennsylvanicus). J. Exp. Biol. 214, 726-734.
28. MacMillan, H. A. and Sinclair, B. J. (2011b). Mechanisms underlying insect chillcoma. J. Insect Physiol. 57, 12-20.
29. Makarieva, A. M., Gorshkov, V. G., Li, B.-L. and Chown, S. L. (2006). Size- and temperature-independence of minimum life-supporting metabolic rates. Funct. Ecol. 20, 83-96.
30. Martins, E. G., Hinch, S. G., Patterson, D. A., Hague, M. J., Cooke, S. J., Miller, K. M., Lapointe, M. F., English, K. K. and Farrell, A. P. (2011). Effects of river temperature and climate warming on stock-specific survival of adult migrating Fraser River sockeye salmon (Oncorhynchus nerka). Glob. Change Biol. 17, 99-114.
31. Melzner, F., Mark, F. C. and Pörtner, H.-O. (2007). Role of blood-oxygen transport in thermal tolerance of the cuttlefish, Sepia officinalis. Integr. Comp. Biol. 47, 645-655.
32. Noll, F. (1984). L-Lactate. In Methods of Enzymatic Analysis: Metabolites, Vol. VI, 3rd edn (ed. H. U. Bergmeyer), pp. 582-588. Weimheim: Verlag Chemie.
33. Nyamukondiwa, C. and Terblanche, J. S. (2010). Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short-term responses to temperature. Physiol. Entomol. 35, 255-264.
34. Overgaard, J., Malmendal, A., Sørensen, J. G., Bundy, J. G., Loeschcke, V., Nielsen, N. C. and Holmstrup, M. (2007). Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J. Insect Physiol. 53, 1218-1232.
35. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and R Development Core Team (2011). nlme: linear and non-linear mixed effects models. R package version 3.1-102.
36. Pörtner, H.-O. (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.
37. Pörtner, H. O. and Knust, R. (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95-97.
38. Pörtner, H. O., Mark, F. C. and Bock, C. (2004). Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir. Physiol. Neurobiol. 141, 243-260.
39. R Development Core Team (2011). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org.
40. Rakshpal, R. (1962). Diapause in the eggs of Gryllus pennsylvanicus Burmeister (Orthoptera: Gryllidae). Can. J. Zool. 40, 179-194.
41. Rodgers, C. I., Armstrong, G. A. B. and Robertson, R. M. (2010). Coma in response to environmental stress in the locust: a model for cortical spreading depression. J. Insect Physiol. 56, 980-990.
42. Schröer, M., Wittmann, A. C., Grüner, N., Steeger, H.-U., Bock, C., Paul, R. and Pörtner, H.-O. (2009). Oxygen limited thermal tolerance and performance in the lugworm Arenicola marina: a latitudinal comparison. J. Exp. Mar. Biol. Ecol. 372, 22-30.
43. Sinclair, B. J., Klok, C. J. and Chown, S. L. (2004). Metabolism of the sub-Antarctic caterpillar Pringleophaga marioni during cooling, freezing and thawing. J. Exp. Biol. 207, 1287-1294.
44. Staszak, D. and Mutchmor, J. A. (1973). Influence of temperature on induction of chill-coma and movement of American cockroach, Periplaneta americana. Comp. Biochem. Physiol. 45A, 895-908.
45. Stevens, M. M., Jackson, S., Bester, S. A., Terblanche, J. S. and Chown, S. L. (2010). Oxygen limitation and thermal tolerance in two terrestrial arthropod species. J. Exp. Biol. 213, 2209-2218.
46. Terblanche, J. S., Deere, J. A., Clusella-Trullas, S., Janion, C. and Chown, S. L. (2007). Critical thermal limits depend on methodological context. Proc. Biol. Sci. 274, 2935-2942.
47. Terblanche, J. S., Clusella-Trullas, S., Deere, J. A. and Chown, S. L. (2008). Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. J. Insect Physiol. 54, 114-127.
48. Van Dijk, P. L. M., Tesch, C., Hardewig, I. and Pörtner, H. O. (1999). Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J. Exp. Biol. 202, 3611-3621.
49. Verberk, W. C. E. P., Bilton, D. T., Calosi, P. and Spicer, J. I. (2011). Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns. Ecology 92, 1565-1572.
50. Williams, C. M., Pelini, S. L., Hellmann, J. J. and Sinclair, B. J. (2010). Intraindividual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects. Biol. Lett. 6, 274-277.
51. Williamson, J. R. (1990). L-Alanine determination with alanine aminotransferase. In Methods of Enzymatic Analysis, Metabolites III: Lipids, Amino Acids and Related Compounds, Vol. VIII, 3rd edn (ed. H. U. Bergmeyer), pp. 345-347. Weimheim: Verlag Chemie.
52. Zielinski, S. and Pörtner, H. O. (1996). Energy metabolism and ATP free-energy change of the intertidal worm Sipunculus nudus below a critical temperature. J. Comp. Physiol. B 166, 492-500.