Osmoregulation and salinity tolerance in the antarctic midge, belgica antarctica: seawater exposure confers enhanced tolerance to freezing and dehydration

Journal of Experimental Biology

Volumn 212, Issue 17, 2009, Pages 2864-2871

  Elnitsky, Michael A ^a,b   Benoit, Joshua B ^c   Lopez Martinez, Giancarlo ^c   Denlinger, David L ^c   Lee Jr , Richard E ^b  

^a MERCYHURST COLLEGE   (United States)

^b MIAMI UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Antarctica; Chironomidae; Cold hardiness; Dehydration; Osmotic stress

Indexed keywords

OXYGEN; SEA WATER;

ACCLIMATIZATION; ANIMAL; ANTARCTICA; ARTICLE; CHIRONOMIDAE; DESICCATION; ELECTROLYTE BALANCE; FREEZING; HEAT SHOCK RESPONSE; LARVA; METABOLISM; PHYSIOLOGY; SALT TOLERANCE;

ACCLIMATIZATION; ANIMALS; ANTARCTIC REGIONS; CHIRONOMIDAE; DESICCATION; FREEZING; HEAT-SHOCK RESPONSE; LARVA; OXYGEN; SALT-TOLERANCE; SEAWATER; WATER-ELECTROLYTE BALANCE;

BELGICA ANTARCTICA; CHIRONOMIDAE;

EID: 70349255676     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.034173     Document Type: Article

References (42)

1. Baust, J. G. and Edwards, J. S. (1979). Mechanisms of freezing tolerance in an Antarctic midge, Belgica antarctica. Physiol. Entomol. 4, 1-5
2. Baust, J. G. and Lee, R. E. (1981), Environmental "homeothermy" In an Antarctic insect, Antarct. J. US 15, 170-172
3. Baust, J. G. and Lee, R. E. (1987), Multiple stress tolerance in an Antarctic terrestrial arthropod: Belgica antarctica. Cryobiology 24, 140-147
4. Bayley, M., Petersen, S. O., Knlgge, T., Kohler, H. R. and Holmstrup, M. (2001), Drought acclimation confers cold tolerance in the soli collembolan Folsomia candida. J. Insect Physiol. 47, 1197-1204
5. Bayly, I. A. E. (1972), Salinity tolerance and osmotic behavior of animals in Athalassic saline and marine hypersallne waters, Annu. Rev. Ecol. Syst. 3, 233-268
6. Benoit, J. B., Lopez-Martinez, G., Mlchaud, M. R., Elnltsky, M. A., Lee, R. E. and Denllnger, D. L. (2007), Mechanisms to reduce dehydration stress in the Antarctic midge, Belgica antarctica. J. Insed Physiol. 53, 656-667
7. Bradley, T. J. (1987), Physiology of osmoregulation In mosquitoes, Annu. Rev. Entomol. 32, 439-462
8. Bradley, T. J. (1994), The role of physiological capacity, morphology and phylogeny in determining habitat use in mosquitoes, In Ecological Morphology: Integrative Organismal Biology (ed. P. C. Wainwright and S. M. Reilly), pp. 303-318. Chicago, IL: University of Chicago Press
9. Chen, Q., Ma, E., Behar, K. L., Xu, T. and Haddad, G. G. (2002), Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster. J. Biol. Chem. 277, 3274-3279
10. Convey P. Block W. Antarctic Diptera: Ecology, physiology and distribution European Journal of Entomology 1996 93 1 1-13 Convey, P. and Block, W. (1996), Antarctic Diptera: ecology, physiology and distribution, Eur. J. Entomol. 93, 1-13 (Pubitemid 2622453)
11. Crowe, J. H., Crowe, L. M. and Chapman, D. (1984), Preservation of membranes in anhydrobiotic organisms: the role of trehalose, Science 223, 701-703
12. Crowe, J. H., Hoekstra, F. A. and Crowe, L. M. (1992), Anhydrobiosis, Annu. Rev. Physiol. 54, 579-599,
13. Elnitsky, M. A., Hayward, S. A. L., Rlnehart, J. P., Denllnger, D. L. and Lee, R. E. (2008), Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge Belgica antarctica. J. Exp. Biol. 211, 524-530
14. Garrett, M. A. and Bradley, T. J. (1987), Extracellular accumulation of proline, serine and trehalose In the haemolymph of osmoconforming brackish-water mosquitoes, J. Exp. Biol. 129, 231-238
15. Hadley, N. F. (1994), Water Relations of Terrestrial Arthropods. San Diego, CA: Academic Press
16. Hawes, T. C. Worland, M. R., Bale, J. S. and Convey, P. (2008), Rafting in Antarctic Collembola, J. Zool. 274, 44-50
17. Hayward, S. A. L., Rlnehart, J. P., Sandro, L. H., Lee, R. E. and Denllnger, D. L. (2007), Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. J. Exp. Biol. 210, 836-844
18. Hochachka, P. W. and Somero, G. N. (2002), Biochemical Adaptation. New York: Oxford University Press
19. Holmstrup M. Somme L. Dehydration and cold hardiness in the Arctic Collembolan Onychiurus arcticus Tullberg 1876 Journal of Comparative Physiology - B Biochemical, Systemic, and Environmental Physiology 1998 168 3 197-203 DOI 10.1007/s003600050137 Holmstrup, M. and Sømme, L. (1998), Dehydration and cold hardiness in the Arctic collembolan Onychiurus arcticus Tullberg 1876. J. Comp. Physiol. B 168, 197-203 (Pubitemid 28213853)
20. Holmstrup M. Costanzo J.P. Lee R.E. Jr. Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms Journal of Comparative Physiology - B Biochemical, Systemic, and Environmental Physiology 1999 169 3 207-214 DOI 10.1007/s003600050213 Holmstrup, M., Costanzo, J. P. and Lee, R. E. (1999), Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms, J. Comp. Physiol. B 169, 207-214 (Pubitemid 29221143)
21. Holmstrup M. Hedlund K. Boriss H. Drought acclimation and lipid composition in Folsomia candida: Implications for cold shock, heat shock and acute desiccation stress Journal of Insect Physiology 2002 48 10 961-970 DOI 10.1016/S0022-1910(02)00175-0, PII S0022191002001750 Holmstrup, M., Hedlund, K. and Borlss, H. (2002), Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress, J. Insed Physiol. 48, 961-970 (Pubitemid 35280870)
22. Irwin S. Wall V. Davenport J. Measurement of temperature and salinity effects on oxygen consumption of Artemia franciscana K., measured using fibre-optic oxygen microsensors Hydrobiologia 2007 575 1 109-115 DOI 10.1007/s10750-006-0358-y Irwin, S., Wall, V. and Davenport, J. (2007), Measurement of temperature and salinity effects on oxygen consumption of Artemia franciscana K., measured using fibre-optic oxygen microsensors, Hydrobiologia 575, 109-115 (Pubitemid 44900417)
23. Kokkinn, M. J. (1986), Osmoregulation, salinity tolerance and the site of ion excretion in the halobiont chironomid, Tanytarsus baritarsis Freeman, Aust. J. Mar. Fresh. Res. 37, 243-250
24. Lee, R. E. (1991), Principles of insect low temperature tolerance, In Insects at Low Temperature (ed. R. E. Lee and D. L. Denlinger), pp. 17-46. New York: Chapman & Hall
25. Lee, R. E., Elnitsky, M. A., Rlnehart, J. P., Hayward, S. A. L., Sandro, L. H. and Denlinger, D. L. (2006), Rapid cold-hardening increases the freezing tolerance of the Antarctic midge, Bélgica antarctica. J. Exp. Biol. 209, 399-406
26. Mlchaud, M. R., Benoit, J. B., Lopez-Martinez, G., Elnitsky, M. A., Lee, R. E. and Denlinger, D. L. (2008), Metabolomics reveals unique and shared metabolic changes In response to heat shock, freezing, and desiccation in the Antarctic midge, Belgica antarctica. J. Insed Physiol. 54, 645-655.
27. Mulr, T. J., Costanzo, J. P. and Lee, R. E. (2007), Osmotic and metabolic responses to dehydration and urea-loading in a dormant, terrestrially hibernating frog, J. Comp. Physiol. B 177, 917-926
28. Neumann, D. (1976), Adaptations of chironomids to intertidal environments, Annu. Rev. Entomol. 21, 387-414
29. Ordiano A. Alvarez F. Alcaraz G. Osmoregulation and oxygen consumption of the hololimnetic prawn, Macrobrachium tuxtlaense at varying salinities (Decapoda, Palaemonidae) Crustaceana 2005 78 8 1013-1022 DOI 10.1163/156854005775197316 Ordlano, A., Alvarez, F. and Alcaraz, G. (2005), Osmoregulation and oxygen consumption of the hololimnetlc prawn, Macrobrachium tuxtlaense at varying salinities (Decapoda, Palaemonidae), Crustaceana 78, 1013-1022 (Pubitemid 46456006)
30. Patrick, M. L. and Bradley, T. J. (2000), The physiology of salinity tolerance in larvae of two species of Culex mosquitoes: the role of compatible solutes, J. Exp. Biol. 203, 821-830
31. Plaut, I. (1999), Effects of salinity acclimation on oxygen consumption in the freshwater blenny, Salaria fluviatilis, and the marine peacock blenny, S. pavo. Mar. Freshw. Res. 50, 655-659
32. Ring, R. A. and Danks, H. V. (1994), Desiccation and cryoprotection: overlapping adaptations, Cryo Letters 15, 181-190
33. Ring, R. A. and Danks, H. V. (1998), The role of trehalose in cold-hardiness and desiccation, Cryo Letters 19, 275-282
34. Sano F. Asakawa N. Inoue Y. Sakurai M. A dual role for intracellular trehalose in the resistance of yeast cells to water stress Cryobiology 1999 39 1 80-87 DOI 10.1006/cryo.1999.2188 Sano, R., Asakawa, N., Inoue, Y. and Sakural, M. (1999), A dual role for intracellular trehalose in the resistance of yeast cells to water stress, Cryobiology 39, 80-87 (Pubitemid 29436839)
35. Sjursen H. Bayley M. Holmstrup M. Enhanced drought tolerance of a soil-dwelling springtail by pre-acclimation to a mild drought stress Journal of Insect Physiology 2001 47 9 1021-1027 DOI 10.1016/S0022-1910(01)00078-6, PII S0022191001000786 SJursen, H., Bayley, M. and Holmstrup, M. (2001), Enhance drought tolerance of a soil-dwelling springtail by pre-acclimation to a mild drought stress, J. Insect Physiol. 47, 1021-1027 (Pubitemid 32737657)
36. Somero, G. N. and Yancey, P. H. (1997), Osmolytes and cell-volume regulation: physiological and evolutionary principles, In The Handbook of Physiology, Section 14: Cell Physiology (ed. J. F. Hoffman and J, D, Jamieson), pp. 441-484. New York: Oxford University Press.
37. Stobbart, R. H. and Shaw, J. (1974), Salt and water balance: excretion, In The Physiology of lnsecta (ed. M. Rockstein), pp. 362-446. New York: Academic Press.
38. Sugg P. Edwards J.S. Baust J. Phenology and life history of Belgica antarctica, an Antarctic midge ( Diptera: Chironomidae). Ecological Entomology 1983 8 1 105-113 Sugg, P., Edwards, J. S. and Baust, J. (1983), Phenology and life history of Belgica antarctica, an Antarctic midge (Diptera: Chironomidae), Ecol. Entomol. 8, 105-113 (Pubitemid 14272189)
39. Usher, M. B. and Edwards, M. (1984), A dipteran from south of the Antarctic Circle: Belgica antarctica (Chironomidae), with a description of its larva, Biol. J. Linn. Soc. 23, 19-31
40. Worland, M. R., Grubor-Lajslc, G. and Montlel, P. O. (1998), Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg), J. Insect Physiol. 44, 211-219
41. Yancey, P. H. (2001), Water stress, osmolytes and proteins, Am. Zool. 41, 699-709
42. Yancey, P. H. (2005), Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses, J. Exp. Biol. 208, 2819-2830