The rapid cold hardening response of Collembola is influenced by thermal variability of the habitat

Functional Ecology

Volumn 23, Issue 2, 2009, Pages 340-347

  Bahrndorff, Simon ^a,b   Loeschcke, Volker ^a   Pertoldi, Cino ^a,c   Beier, Claus ^d   Holmstrup, Martin ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b Natural History Museum   (Denmark)

^c MAMMAL RESEARCH INSTITUTE   (Poland)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Clinal variation; Coefficient of variation; Cold shock tolerance; Phylogenetic signal; Springtails; Thermal adaptation; Thermal autocorrelation

Indexed keywords

ACCLIMATION; AUTOCORRELATION; CLINE; COLD TOLERANCE; COMPARATIVE STUDY; ENVIRONMENTAL CHANGE; ENVIRONMENTAL STRESS; GEOGRAPHICAL DISTRIBUTION; HABITAT QUALITY; INSECT; PHYLOGENETICS; PHYSIOLOGY;

COLLEMBOLA; ORCHESELLA CINCTA;

EID: 62449099796     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2008.01503.x     Document Type: Article

References (55)

1. Abouheif, E. (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evolutionary Ecology Research, 1, 895 909.
2. Addo-Bediako, A., Chown, S.L. Gaston, K.J. (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London Series B - Biological Sciences, 267, 739 745.
3. Bahrndorff, S., Holmstrup, M., Petersen, H. Loeschcke, V. (2006) Geographic variation for climatic stress resistance traits in the springtail Orchesella cincta. Journal of Insect Physiology, 52, 951 959.
4. Bahrndorff, S., Petersen, S.O., Loeschcke, V., Overgaard, J. Holmstrup, M. (2007) Differences in cold and drought tolerance of high arctic and subarctic populations of Megaphorura arctica Tullberg 1876 (Onychiuridae: Collembola). Cryobiology, 55, 323.
5. Bale, J.S. (1993) Classes of insect cold-hardiness. Functional Ecology, 7, 751 753.
6. Beier, C., Emmett, B., Gundersen, P., Tietema, A., Penuelas, J., Estiarte, M., Gordon, C., Gorissen, A., Llorens, L., Roda, F. Williams, D. (2004) Novel approaches to study climate change effects on terrestrial ecosystems in the field: drought and passive nighttime warming. Ecosystems, 7, 583 597.
7. Block, W. (2003) Water or ice? - the challenge for invertebrate cold survival. Science Progress, 86, 77 101.
8. Chen, C.P. Walker, V.K. (1993) Increase in cold-shock tolerance by selection of cold resistant lines in Drosophila melanogaster. Ecological Entomology, 18, 184 190.
9. Chen, C.P., Denlinger, D.L. Lee, R.E. (1987) Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiological Zoology, 60, 297 304.
10. Chen, C.P., Lee, R.E. Denlinger, D.L. (1990) A comparison of the responses of tropical and temperate flies (Diptera, Sarcophagidae) to cold and heat-stress. Journal of Comparative Physiology B - Biochemical Systemic and Environmental Physiology, 160, 543 547.
11. Chown, S.L. Terblanche, J.S. (2007) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology, 33, 50 152.
12. Chown, S.L., Addo-Bediako, A. Gaston, K.J. (2002) Physiological variation in insects: large-scale patterns and their implications. Comparative Biochemistry and Physiology B - Biochemistry and Molecular Biology, 131, 587 602.
13. Coulson, S.J., Hodkinson, I.D., Block, W., Webb, N.R. Worland, M.R. (1995) Low summer temperatures - a potential mortality factor for high arctic soil microarthropods. Journal of Insect Physiology, 41, 783 792.
14. Czajka, M.C. Lee, R.E. (1988) Cold shock and rapid cold hardening in Drosophila melanogaster. Cryobiology, 25, 546.
15. Czajka, M.C. Lee, R.E. (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. Journal of Experimental Biology, 148, 245 254.
16. Deere, J.A. Chown, S.L. (2006) Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. American Naturalist, 168, 630 644.
17. Donnelly, S.M. Kramer, A. (1999) Testing for multiple species in fossil samples: an evaluation and comparison of tests for equal relative variation. American Journal of Physical Anthropology, 108, 507 529.
18. Folmer, O., Black, M., Hoeh, W., Lutz, R. Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294 299.
19. Garcia, L.V. (2003) Controlling the false discovery rate in ecological research. Trends in Ecology and Evolution, 18, 553 554.
20. Gaston, K.J., Chown, S.L. Evans, K.L. (2008) Ecogeographical rules: elements of a synthesis. Journal of Biogeography, 35, 483 500.
21. Gittleman, J.L. Kot, M. (1990) Adaptation - statistics and a null model for estimating phylogenetic effects. Systematic Zoology, 39, 227 241.
22. Hammer, Ø., Harper, D.A.T. Ryan, P.D. (2001) past: Palaeontological Statistics software package for education and data analysis. Palaeontologica Electronica, 4, 9.
23. Harshman, L.G. Hoffmann, A.A. (2000) Laboratory selection experiments using Drosophila: what do they really tell us? Trends in Ecology and Evolution, 15, 32 36.
24. Hawes, T.C., Couldridge, C.E., Bale, J.S., Worland, M.R. Convey, P. (2006) Habitat temperature and the temporal scaling of cold hardening in the high Arctic collembolan, Hypogastrura tullbergi (Schaffer). Ecological Entomology, 31, 450 459.
25. Hoffmann, A.A., Sørensen, J.G. Loeschcke, V. (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology, 28, 175 216.
26. Hogg, I.D. Hebert, P.D.N. (2004) Biological identification of springtails (Hexapoda: Collembola) from the Canadian Arctic, using mitochondrial DNA barcodes. Canadian Journal of Zoology - Revue Canadienne de Zoologie, 82, 749 754.
27. Holmstrup, M., Bayley, M. Ramløv, H. (2002) Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. Proceedings of the National Academy of Sciences of the United States of America, 99, 5716 5720.
28. Joosse, E.N.G. Verhoef, H.A. (1987) Developments in ecophysiological research on soil invertebrates. Advances in Ecological Research, 16, 175 248.
29. Joplin, K.H., Yocum, G.D. Denlinger, D.L. (1990) Cold shock elicits expression of heat-shock proteins in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology, 36, 825 834.
30. Kærsgaard, C.W., Holmstrup, M., Malte, H. Bayley, M. (2004) The importance of cuticular permeability, osmolyte production and body size for the desiccation resistance of nine species of Collembola. Journal of Insect Physiology, 50, 5 15.
31. Kelty, J.D. Lee, R.E. (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. Journal of Insect Physiology, 45, 719 726.
32. Kelty, J.D. Lee, R.E. (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera : Drosophilidae) during ecologically based thermoperiodic cycles. Journal of Experimental Biology, 204, 1659 1666.
33. Kostal, V., Vambera, J. 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. Journal of Experimental Biology, 207, 1509 1521.
34. Lee, R.E., Chen, C.P. Denlinger, D.L. (1987a) A rapid cold-hardening process in insects. Science, 238, 1415 1417.
35. Lee, R.E., Chen, C.P. Denlinger, D.L. (1987b) Cold shock and rapid cold-hardening in nonoverwintering insects. Cryobiology, 24, 569.
36. Lee, R.E., Damodaran, K., Yi, S.X. Lorigan, G.A. (2006) Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology, 52, 459 463.
37. Martins, E.P. Hansen, T.F. (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist, 149, 646 667.
38. Michaud, M.R. Denlinger, D.L. (2006) Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology, 52, 1073 1082.
39. Overgaard, J., Malmendal, A., Sorensen, J.G., Bundy, J.G., Loeschcke, V., Nielsen, N.C. Holmstrup, M. (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. Journal of Insect Physiology, 53, 1218 1232.
40. Overgaard, J., Sørensen, J.G., Petersen, S.O., Loeschcke, V. Holmstrup, M. (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology, 51, 1173 1182.
41. Powell, S.J. Bale, J.S. (2004) Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera : Aphididae). Journal of Insect Physiology, 50, 277 284.
42. Reeve, J. Abouheif, E. Phylogenetic independence. (Version 1.1. [l.I]) 1999) Department of Ecology and Evolution, SUNY at Stony Brook.
43. Shreve, S.M., Kelty, J.D. Lee, R.E. (2004) Preservation of reproductive behaviors during modest cooling: rapid cold-hardening fine-tunes organismal response. Journal of Experimental Biology, 207, 1797 1802.
44. Sinclair, B.J. (1999) Insect cold tolerance: how many kinds of frozen? European Journal of Entomology, 96, 157 164.
45. Sinclair, B.J., Klok, C.J., Scott, M.B., Terblanche, J.S. Chown, S.L. (2003a) Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica. Journal of Insect Physiology, 49, 1049 1061.
46. Sinclair, B.J., Vernon, P., Klok, C.J. Chown, S.L. (2003b) Insects at low temperatures: an ecological perspective. Trends in Ecology and Evolution, 18, 257 262.
47. Slabber, S., Worland, M.R., Leinaas, H.P. Chown, S.L. (2007) Acclimation effects on thermal tolerances of springtails from sub-Antarctic Marion Island: Indigenous and invasive species. Journal of Insect Physiology, 53, 113 125.
48. Sømme, L. (1982) Supercooling and winter survival in terrestrial arthropods. Comparative Biochemistry and Physiology A - Physiology, 73, 519 543.
49. Stevens, G.C. (1989) The latitudinal gradient in geographical range - how so many species coexist in the tropics. American Naturalist, 133, 240 256.
50. Stevens, G.C. (1992) The elevational gradient in altitudinal range - an extension of rapoport latitudinal rule to altitude. American Naturalist, 140, 893 911.
51. Tang, M., Waring, A.J. Hong, M. (2007) Trehalose-protected lipid membranes for determining membrane protein structure and insertion. Journal of Magnetic Resonance 184, 222 227.
52. Terblanche, J.S., Deere, J.A., Clusella-Trullas, S., Janion, C. Chown, S.L. (2007) Critical thermal limits depend on methodological context. Proceedings of the Royal Society B - Biological Sciences, 274, 2935 2942.
53. Willmer, P.G. (1982) Microclimate and the environmental physiology of insects. Advances in Insect Physiology, 16, 1 57.
54. Worland, M.R. Convey, P. (2001) Rapid cold hardening in Antarctic microarthropods. Functional Ecology, 15, 515 524.
55. Worland, M.R., Leinaas, H.P. Chown, S.L. (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Functional Ecology, 20, 323 329.