Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T12:15:52.548Z Has data issue: false hasContentIssue false

Are the Antarctic dipteran, Eretmoptera murphyi, and Arctic collembolan, Megaphorura arctica, vulnerable to rising temperatures?

Published online by Cambridge University Press:  12 May 2014

M.J. Everatt*
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
P. Convey
Affiliation:
British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK National Antarctic Research Center, IPS Building, University Malaya, 50603 Kuala Lumpur, Malaysia Gateway Antarctica, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand
M.R. Worland
Affiliation:
British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK
J.S. Bale
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
S.A.L. Hayward
Affiliation:
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
*
*Author for correspondence Phone: + 44 789 620 1770 E-mail: [email protected]

Abstract

Polar terrestrial invertebrates are suggested as being vulnerable to temperature change relative to lower latitude species, and hence possibly also to climate warming. Previous studies have shown Antarctic and Arctic Collembola and Acari to possess good heat tolerance and survive temperature exposures above 30 °C. To test this feature further, the heat tolerance and physiological plasticity of heat stress were explored in the Arctic collembolan, Megaphorura arctica, from Svalbard and the Antarctic midge, Eretmoptera murphyi, from Signy Island. The data obtained demonstrate considerable heat tolerance in both species, with upper lethal temperatures ≥35 °C (1 h exposures), and tolerance of exposure to 10 and 15 °C exceeding 56 days. This tolerance is far beyond that required in their current environment. Average microhabitat temperatures in August 2011 ranged between 5.1 and 8.1 °C, and rarely rose above 10 °C, in Ny-Ålesund, Svalbard. Summer soil microhabitat temperatures on Signy Island have previously been shown to range between 0 and 10 °C. There was also evidence to suggest that E. murphyi can recover from high-temperature exposure and that M. arctica is capable of rapid heat hardening. M. arctica and E. murphyi therefore have the physiological capacity to tolerate current environmental conditions, as well as future warming. If the features they express are characteristically more general, such polar terrestrial invertebrates will likely fare well under climate warming scenarios.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addo-Bediako, A., Chown, S.L. & Gaston, K.J. (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society of London B 267, 739745.CrossRefGoogle ScholarPubMed
Allegrucci, G., Carchini, G., Convey, P. & Sbordoni, V. (2012) Evolutionary geographic relationships among chironomid midges from maritime Antarctic and sub-Antarctic islands. Biological Journal of the Linnean Society 106, 258274.Google Scholar
Arctic Council (2005) Arctic Climate Impact Assessment – Scientific Report. Cambridge, Cambridge University Press, 1046pp. Available at www.acia.uaf.edu/pages/scientific.html.Google Scholar
Ávila-Jiménez, M.L., Coulson, S.J., Solhøy, T. & Sjöblom, A. (2010) Overwintering of terrestrial Arctic arthropods: the fauna of Svalbard now and in the future. Polar Research 29, 127137.Google Scholar
Bale, J.S. & Hayward, S.A.L. (2010) Insect overwintering in a changing climate. Journal of Experimental Biology 213, 980994.Google Scholar
Benoit, J.B., Lopez-Martinez, G., Elnitsky, M.A., Lee, R.E. & Denlinger, D.L. (2009 a) Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 152, 518523.Google Scholar
Benoit, J.B., Lopez-Martinez, G., Teets, N.M., Phillips, S.A. & Denlinger, D.L. (2009 b) Responses of the bed bug, Cimex lectularius, to temperature extremes and dehydration: levels of tolerance, rapid cold hardening and expression of heat shock proteins. Medical and Veterinary Entomology 23, 418425.Google Scholar
Block, W., Burn, A.J. & Richard, K.J. (1984) An insect introduction to the maritime Antarctic. Biological Journal of the Linnean Society 23, 3339.Google Scholar
Block, W., Webb, N.R., Coulson, S., Hodkinson, I.D. & Worland, M.R. (1994) Thermal adaptation in the Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology 40, 715722.CrossRefGoogle Scholar
Block, W., Smith, R.I.L. & Kennedy, A.D. (2009) Strategies of survival and resource exploitation in the Antarctic fellfield ecosystem. Biological Reviews of the Cambridge Philosophical Society 84, 449–84.Google Scholar
Bokhorst, S., Huiskes, A., Convey, P., van Bodegom, P.M. & Aerts, R. (2008) Climate change effects on soil arthropod communities from the Falkland Islands and the maritime Antarctic. Soil Biology and Biochemistry 40, 15471556.Google Scholar
Bokhorst, S., Huiskes, A., Convey, P., Sinclair, B.J., Lebouvier, M., Van de Vijver, B. & Wall, D.H. (2011) Microclimate impacts of passive warming methods in Antarctica: implications for climate change studies. Polar Biology 34, 14211435.Google Scholar
Bokhorst, S., Huiskes, A., Aerts, R., Convey, P., Cooper, E.J., Dalen, L., Erschbamer, B., Gudmundsson, J., Hofgaard, A., Hollister, R.D., Johnstone, J., Jónsdóttir, I.S., Lebouvier, M., Van de Vijver, B., Wahren, C-H. & Ellen Dorrepaal, E. (2013) Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Global Change Biology 19, 6474.CrossRefGoogle ScholarPubMed
Callaghan, T.V., Sonesson, M., Somme, L., Walton, D.W.H., Christensen, T. and Block, W. (1992) Responses of terrestrial plants and invertebrates to environmental change at high latitudes [and discussion]. Philosophical Transactions of the Royal Society of London B 338, 279288.Google Scholar
Chown, S.L., Lee, J.E., Hughes, K.A., Barnes, J., Barrett, P.J., Bergstrom, D.M., Convey, P., Cowan, D.A., Crosbie, K., Dyer, G., Frenot, Y., Grant, S.M., Herr, D., Kennicutt, M.C. II, Lamers, M., Murray, A., Possingham, H.P., Reid, K. & Riddle, M.J. (2012) Challenges to the future conservation of the Antarctic. Science 337, 158159.CrossRefGoogle Scholar
Chwedorzewska, K. (2009) Terrestrial Antarctic ecosystems in the changing world: an overview. Polish Polar Science 30, 263276.Google Scholar
Clark, M.S. & Worland, M.R. (2008) How insects survive the cold: molecular mechanisms – a review. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 178, 917–33.CrossRefGoogle ScholarPubMed
Colinet, H. (2011) Disruption of ATP homeostasis during chronic cold stress and recovery in the chill susceptible beetle (Alphitobius diaperinus). Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 160, 6367.CrossRefGoogle ScholarPubMed
Colinet, H., Hance, T., Vernon, P., Bouchereau, A. & Renault, D. (2007) Does fluctuating thermal regime trigger free amino acid production in the parasitic wasp Aphidus colemani (Hymenoptera: Aphidiinae). Comparative Biochemistry and Physiology – Part A 147, 484492.Google Scholar
Colinet, H., Lalouette, L. & Renault, D. (2011) A model for the time-temperature-mortality relationship in the chill-susceptible beetle, Alphitobius diaperinus, exposed to fluctuating thermal regimes. Journal of Thermal Biology 36, 403408.CrossRefGoogle Scholar
Convey, P. (1996) Overwintering strategies of terrestrial invertebrates in Antarctica – the significance of flexibility in extremely seasonal environments. European Journal of Entomology 93, 489505.Google Scholar
Convey, P. (2006) Antarctic climate change and its influences on terrestrial ecosystems. pp. 253272 in Bergstrom, D.M., Convey, P. & Huiskes, A.H.L. (Eds) Trends in Antarctic Terrestrial and Limnetic Ecosystems: Antarctica as a Global Indicator. Dordrecht, Springer.Google Scholar
Convey, P. (2011) Antarctic terrestrial biodiversity in a changing world. Polar Biology 34, 16291641.Google Scholar
Convey, P. & Block, W. (1996) Antarctic Diptera: ecology, physiology and distribution. European Journal of Entomology 93, 113.Google Scholar
Convey, P. & Worland, M.R. (2000) Refining the risk of freezing mortality for Antarctic terrestrial microarthropods. Cryoletters 21, 333338.Google ScholarPubMed
Convey, P. & Wynn-Williams, D.D. (2002) Antarctic soil nematode response to artificial climate amelioration. European Journal of Soil Biology 38, 255259.CrossRefGoogle Scholar
Convey, P., Pugh, P.J.A., Jackson, C., Murray, A.W., Ruhland, C.T., Xiong, F.S. & Day, A. (2002) Response of Antarctic terrestrial microarthropods to long-term climate manipulations. Ecology 83, 31303140.CrossRefGoogle Scholar
Convey, P., Block, W. & Peat, H.J. (2003) Soil arthropods as indicators of water stress in Antarctic terrestrial habitats? Global Change Biology 9, 718730.Google Scholar
Convey, P., Bindschadler, R., di Prisco, G., Fahrbach, E., Gutt, J., Hodgson, D.A., Mayewski, P.A., Summerhayes, C.P. & Turner, J. (2009) Antarctic climate change and the environment. Antarctic Science 21, 541563.Google Scholar
Coulson, S.J., Hodkinson, I.D., Webb, N.R., Block, W., Bale, J.S., Strathdee, A.T., Worland, M.R. & Wooley, C. (1996) Effects of experimental temperature elevation on high-arctic soil microarthropod populations. Polar Biology 16, 147153.CrossRefGoogle Scholar
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, 245254.Google Scholar
Davey, M.C., Pickup, J. & Block, W. (1992) Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island. Antarctic Science 4, 383388.CrossRefGoogle Scholar
Day, T.A., Ruhland, C.T., Strauss, S.L., Park, J., Krieg, M.L., Krna, M.A. & Bryant, D.M. (2009) Response of plants and the dominant microarthropod, Cryptopygus antarcticus, to warming and contrasting precipitation regimes in Antarctic tundra. Global Change Biology 15, 16401651.CrossRefGoogle Scholar
Deere, J.A., Sinclair, B.J., Marshall, D.J. & Chown, S.L. (2006) Phenotypic plasticity of thermal tolerances in five oribatid mite species from sub-Antarctic Marion Island. Journal of Insect Physiology 52, 693700.Google Scholar
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. & Martin, P.R. (2008) Impacts of climate warming on terrestrial ectotherms across latitude thermal safety margin. Proceedings of the National Academy of Sciences 105, 66686672.Google Scholar
Dollo, V.H., Yi, S.X. & Lee, R.E. Jr. (2010) High temperature pulses decrease indirect chilling injury and elevate ATP levels in the flesh fly, Sarcophaga crassipalpis . Cryobiology 60, 351353.CrossRefGoogle ScholarPubMed
Everatt, M.J., Worland, M.R., Bale, J.S., Convey, P. & Hayward, S.A.L. (2012) Pre-adapted to the maritime Antarctic? – Rapid cold hardening of the midge, Eretmoptera murphyi . Journal of Insect Physiology 58, 11041111.Google Scholar
Everatt, M.J., Convey, P., Worland, M.R., Bale, J.S. & Hayward, S.A.L. (2013) Heat tolerance and physiological plasticity in the Antarctic collembolan, Cryptopygus antarcticus, and the mite, Alaskozetes antarcticus . Journal of Thermal Biology 38, 264271.Google Scholar
Fjellberg, A. (1994) The Collembola of the Norwegian Arctic Islands. Meddelelser 133. Oslo, Norsk Polar Institute.Google Scholar
Frenot, Y., Chown, S.L., Whinam, J., Selkirk, P.M., Convey, P., Skotnicki, M. & Bergstrom, D.M. (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews of the Cambridge Philosophical Society 80, 4572.Google Scholar
Hayward, S.A.L., Worland, M.R., Convey, P. & Bale, J.S. (2003) Temperature preferences of the mite, Alaskozetes antarcticus, and the collembolan, Cryptopygus antarcticus from the maritime Antarctic. Physiological Entomology 28, 114121.Google Scholar
Hayward, S.A.L., Rinehart, J.P., Sandro, L.H., Lee, R.E. & Denlinger, D.L. (2007) Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica . Journal of Experimental Biology 210, 836844.Google Scholar
Hazell, S.P., Pedersen, B.P., Worland, M.R., Blackburn, T.M. & Bale, J.S. (2008) A method for the rapid measurement of thermal tolerance traits in studies of small insects. Physiological Entomology 33, 389394.Google Scholar
Hodkinson, I.D., Coulson, S.J., Webb, N.R. & Block, W. (1996) Can high Arctic soil microarthropods survive elevated summer temperatures? Functional Ecology 10, 314321.Google Scholar
Hughes, K.A., Worland, M.R., Thorne, M.A.S. & Convey, P. (2013) The non-native chironomid Eretmoptera murphyi in Antarctica: erosion of the barriers to invasion. Biological Invasions 15, 269281.CrossRefGoogle Scholar
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, 719–26.Google Scholar
Koštál, V., Renault, D., Mehrabianová, A. & Bastl, J. (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology A 147, 231238.Google Scholar
Lalouette, L., Williams, C.M., Hervant, F., Sinclair, B.J. & Renault, D. (2011) Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations. Comparative Biochemistry and Physiology A 158, 229234.Google Scholar
Lee, R.E., Chen, C.P. & Denlinger, D.L. (1987) A rapid cold-hardening process in insects. Science (New York, NY) 238, 1415–17.Google Scholar
Lee, R.E., Elnitsky, M.A., Rinehart, J.P., Hayward, S.A.L., Sandro, L.H. & Denlinger, D.L. (2006) Rapid cold-hardening increases the freezing tolerance of the Antarctic midge Belgica antarctica . Journal of Experimental Biology 209, 399406.Google Scholar
McDonald, J.R., Bale, J.S. & Walters, K.F.A. (1997) Rapid cold hardening in the western flower thrips Frankliniella occidentalis . Journal of Insect Physiology 43, 759766.Google Scholar
Owen, E.L., Bale, J.S. & Hayward, S.A.L. (2013) Can winter-active bumblebees survive the cold? Assessing the cold tolerance of Bombus terrestris audax and the effects of pollen feeding. PloS One 8, e80061.Google Scholar
Parmesan, C. (1996) Climate and species range. Nature 382, 765766.CrossRefGoogle Scholar
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, 277–84.Google Scholar
Renault, D., Nedvěd, O., Hervant, F. & Vernon, P. (2004) The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature. Physiological Entomology 29, 139145.Google Scholar
Schulte, G.G., Elnitsky, M.A., Benoit, J.B., Denlinger, D.L. & Lee, R.E. (2008) Extremely large aggregations of collembolan eggs on Humble Island, Antarctica: a response to early seasonal warming? Polar Biology 31, 889892.Google Scholar
Sinclair, B.J., Terblanche, J.S. & Scott, M.B. (2006) Environmental physiology of three species of springtail at Cape Hallett, North Victoria Land, Antarctica. Journal of Insect Physiology 52, 2950.Google Scholar
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, 113125.Google Scholar
Smith, R.I.L. (1988) Recording bryophyte microclimate in remote and severe environments. pp. 275284 in Glime, J.M. (Ed.) Methods in Bryology. Nichinan, Miyazaki, Hattori Botanical Laboratory.Google Scholar
Somero, G. (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology 213, 912920.Google Scholar
Speight, M.R., Hunter, M.D. & Watt, A.D. (2008) Insects and climate. pp. 3360 in Speight, M.R., Hunter, M.D. & Watt, A.D. (Eds) Ecology of Insects Concepts and Applications. Chichester, Wiley-Blackwell.Google Scholar
Tammariello, S.P., Rinehart, J.P. & Denlinger, D.L. (1999) Desiccation elicits heat shock protein transcription in the flesh fly, Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. Journal of Insect Physiology 45, 933938.Google Scholar
Turner, J., Bindschadler, R., Convey, P., Di Prisco, G., Fahrbach, E., Gutt, J., Hodgson, D.A., Mayewski, P.A. & Summerhayes, C.P. (Eds) (2009) Antarctic Climate Change and the Environment. Cambridge, Scientific Committee for Antarctic Research, 554pp.Google Scholar
Walther, G., Post, E., Convey, P., Menzel, A., Parmesank, C., Beebee, T.J.C., Fromentin, J.I., Ove, H. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature 416, 389395.Google Scholar
Webb, N.R., Coulson, S.J., Hodkinson, I.D., Block, W., Bale, J.S., & Strathdee, A.T. (1998) The effects of experimental temperature elevation on populations of cryptostigmatic mites in high Arctic soils. Pedobiologia 42, 298308.Google Scholar
Worland, M.R. (1996) The relationship between water content and cold tolerance in the Arctic collembolan Onychiurus arcticus (Collembola: Onychiuridae). European Journal of Entomology 93, 341348.Google Scholar
Worland, M.R., Grubor-Lajsic, G. & Montiel, P. (1998) Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). Journal of Insect Physiology 44, 211219.Google Scholar
Yi, S-X., Moore, C.W. & Lee, R.E. (2007) Rapid cold-hardening protects Drosophila melanogaster from cold-induced apoptosis. Apoptosis: An International Journal on Programmed Cell Death 12, 1183–93.Google Scholar