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Freeze tolerance of Cyphoderris monstrosa (Orthoptera: Prophalangopsidae)

Published online by Cambridge University Press:  06 June 2016

Jantina Toxopeus ,
Jacqueline E. Lebenzon ,
Alexander H McKinnon  and
Brent J. Sinclair
Jantina Toxopeus*
Affiliation:
Department of Biology, University of Western Ontario, 1151 Richmond Street N, London, Ontario, N6A 5B7, Canada
Jacqueline E. Lebenzon
Affiliation:
Department of Biology, University of Western Ontario, 1151 Richmond Street N, London, Ontario, N6A 5B7, Canada
Alexander H McKinnon
Affiliation:
Department of Biology, University of Western Ontario, 1151 Richmond Street N, London, Ontario, N6A 5B7, Canada
Brent J. Sinclair
Affiliation:
Department of Biology, University of Western Ontario, 1151 Richmond Street N, London, Ontario, N6A 5B7, Canada
*
1Corresponding author (e-mail: jtoxopeu@uwo.ca).
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Abstract

The great grig, Cyphoderris monstrosa Uhler (Orthoptera: Prophalangopsidae), is a large (20–30 mm, >1 g), nocturnal ensiferan that inhabits montane coniferous forests in northwestern North America. Cyphoderris monstrosa overwinters as a late instar nymphs, but its cold tolerance strategy has not previously been reported. We collected nymphs from near Kamloops, British Columbia, Canada in late spring to determine their cold tolerance strategy. Cyphoderris monstrosa nymphs were active at low temperatures until they froze at −4.6±0.3 °C. The nymphs survived internal ice formation (i.e., are freeze tolerant), had a lethal temperature between −9 °C and −12 °C, and could survive for between five and 10 days at −6 °C. Isolated C. monstrosa gut, Malpighian tubules, and metafemur muscle tissues froze at temperatures similar to whole nymphs, and likely inoculate freezing in vivo. Hemolymph osmolality was 358±51 mOsm, with trehalose and proline comprising ~10% of that total. Glycerol was not detectable in hemolymph from field-fresh nymphs, but accumulated after freezing and thawing. The control of ice formation and presence of hemolymph cryoprotectants may contribute to C. monstrosa freeze tolerance and overwintering survival.

Type
Physiology, Biochemistry, Development, and Genetics
Information
The Canadian Entomologist , Volume 148 , Issue 6 , December 2016 , pp. 668 - 672
Copyright
© Entomological Society of Canada 2016 

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Footnotes

Subject Editor: Hervé Colinet

References

Alexander, G. 1967. Cold hardiness in overwintering juvenile grasshoppers. Entomological News, 78: 147–154.Google Scholar
Anand, A.N. and Lorenz, M.W. 2008. Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllus bimaculatus . Journal of Insect Physiology, 54: 1404–1412.Google Scholar
Carillo, P. and Gibon, Y. 2011. Protocol: extraction and determination of proline [online]. Available from: http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Extraction%20and%20determination%20of%20proline&refresh=1 [accessed 20 December 2015].Google Scholar
Caudell, A.N. 1904. The genus Cyphoderris . Journal of the New York Entomological Society, 12: 47–53.Google Scholar
Crosthwaite, J.C., Sobek, S., Lyons, D.B., Bernards, M.A., and Sinclair, B.J. 2011. The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). Journal of Insect Physiology, 57: 166–173.Google Scholar
Ditrich, T. and Koštál, V. 2011. Comparative analysis of overwintering physiology in nine species of semi-aquatic bugs (Heteroptera: Gerromorpha). Physiological Entomology, 36: 261–270.CrossRefGoogle Scholar
Dodson, G.N., Morris, G.K., and Gwynne, D.T. 1983. Mating behavior of the primitive orthopteran genus Cyphoderris (Haglidae). In Orthopteran mating systems: sexual competition in a diverse group of insects. Edited by D.T. Gwynne and G.K. Morris. Westview Press, Boulder, Colorado, United States of America. Pp. 305–318.Google Scholar
Environment Canada. 2015. Historical climate data, Kamloops, British Columbia [online]. Available from http://climate.weather.gc.ca/index_e.html [accessed 4 February 2016].Google Scholar
Gwynne, D.T. 1995. Phylogeny of the Ensifera (Orthoptera): a hypothesis supporting multiple origins of acoustical signalling, complex spermatophores and maternal care in crickets, katydids, and weta. Journal of Orthoptera Research, 4: 203–218.CrossRefGoogle Scholar
Hao, S.-G. and Kang, L. 2004. Supercooling capacity and cold hardiness of the eggs of the grasshopper Chorthippus fallax (Orthoptera: Acrididae). European Journal of Entomology, 101: 231–236.Google Scholar
Kumala, M., McLennan, D.A., Brooks, D.R., and Mason, A.C. 2005. Phylogenetic relationships within hump-winged grigs, Cyphoderris (Insecta, Orthoptera, Tettigonioidea, Haglidae). Canadian Journal of Zoology, 83: 1003–1011.Google Scholar
Ladau, J. 2003. Territoriality and singing-site preferences in the cricket, Cyphoderris monstrosa (Orthoptera: Haglidae) in western North America. Entomological News, 114: 197–204.Google Scholar
Lee, R.E. 2010. A primer on insect cold-tolerance. In Low temperature biology of insects. Edited by D.L. Denlinger and R.E. Lee. Cambridge University Press, New York, New York, United States of America. Pp. 3–34.Google Scholar
MacMillan, H.A. and Sinclair, B.J. 2011. The role of gut in insect chilling injury: cold-induced disruption of osmoregulation in the field fall cricket, Gryllus pennsylvanicus . Journal of Experimental Biology, 214: 726–734.Google Scholar
Marshall, K.E. and Sinclair, B.J. 2015. The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect. Functional Ecology, 29: 357–366.Google Scholar
Mason, A.C. 1996. Territoriality and the function of song in the primitive acoustic insect Cyphoderris monstrosa (Orthoptera: Haglidae). Animal Behaviour, 51: 211–214.Google Scholar
McKinnon, A.H. 2015. Freeze tolerance in the spring field cricket, Gryllus veletis. M.Sc. thesis. University of Western Ontario, London, Ontario, Canada.Google Scholar
Morris, G.K. and Gwynne, D.T. 1978. Geographical distribution and biological observations of Cyphoderris (Orthoptera: Haglidae) with a description of a new species. Psyche, 85: 147–167.CrossRefGoogle Scholar
Morris, G.K., Gwynne, D.T., Klimas, D.E., and Sakaluk, S.K. 1989. Virgin male mating advantage in a primitive acoustic insect (Orthoptera: Haglidae). Journal of Insect Behavior, 2: 173–185.Google Scholar
Mugnano, J.A., Lee, R.E., and Taylor, R.T. 1996. Fat body cells and calcium phosphate spherules induce ice nucleation in the freeze-tolerant larve of the gall fly Eurosta solidaginis (Diptera, Tephritidae). Journal of Experimental Biology, 199: 465–471.Google Scholar
Neufeld, D.S. and Leader, L.P. 1998. Freezing survival by isolated Malpighian tubules of the New Zealand alpine weta Hemideina maori . Journal of Experimental Biology, 201: 227–236.Google Scholar
Petty, S.K., Zuckerberg, B., and Pauli, J.N. 2015. Winter conditions and land cover structure the subnivium, a seasonal refuge beneath the snow. PLoS One, 10: e0127613.Google Scholar
R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org [accessed 21 March 2016].Google Scholar
Ramløv, H. 1999. Microclimate and variations in haemolymph composition in the freezing-tolerant New Zealand alpine weta Hemideina maori Hutton (Orthoptera: Stenopelmatidae). Journal of Comparative Physiology B, 169: 224–235.Google Scholar
Ramløv, H., Bedford, J., and Leader, J. 1992. Freezing tolerance of the New Zealand alpine weta, Hemideina maori Hutton [Orthoptera; Stenopelmatidae]. Journal of Thermal Biology, 17: 51–54.Google Scholar
Ramløv, H. and Westh, P. 1993. Ice formation in the freeze tolerant alpine weta Hemideina maori Hutton (Orthoptera, Stenopelmatidae). Cryo-Letters, 14: 169–176.Google Scholar
Sinclair, B.J., Addo-Beddiako, A., and Chown, S.L. 2003. Climatic variability and the evolution of insect freeze tolerance. Biological Reviews, 78: 181–195.Google Scholar
Sinclair, B.J., Alvarado, L.E.C., and Ferguson, L.V. 2015. An invitation to measure insect cold tolerance: methods, approaches, and workflow. Journal of Thermal Biology, 53: 180–197.CrossRefGoogle ScholarPubMed
Sinclair, B.J., Gibbs, A.G., Lee, W.-K., Rajamohan, A., Roberts, S.P., and Socha, J.J. 2009. Synchrotron x-ray visualisation of ice formation in insects during lethal and non-lethal freezing. PLoS One, 4: e8259.Google Scholar
Sinclair, B.J., Worland, M.R., and Wharton, D.A. 1999. Ice nucleation and freezing tolerance in New Zealand alpine and lowland weta, Hemideina spp. (Orthoptera; Stenopelmatidae). Physiological Entomology, 24: 56–63.CrossRefGoogle Scholar
Sømme, L. 1986. Tolerance to low temperatures and desiccation in insects from Andean paramos. Arctic and Alpine Research, 18: 253–259.Google Scholar
Tennessen, J.M., Barry, W.E., Cox, J., and Thummel, C.S. 2014. Methods for studying metabolism in Drosophila . Methods, 68: 105–115.Google Scholar
Zachariassen, K.E. and Kristiansen, E. 2000. Ice nucleation and antinucleation in nature. Cryobiology, 41: 257–279.Google Scholar