Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-20T00:10:37.428Z Has data issue: false hasContentIssue false
  • English
  • Français

Cold acclimation increases cold tolerance independently of diapause programing in the bean bug, Riptortus pedestris

Published online by Cambridge University Press:  17 October 2017

J. Rozsypal ,
M. Moos  and
S.G. Goto
J. Rozsypal*
Affiliation:
Institute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic Graduate School of Science, Osaka City University, Osaka, Japan
M. Moos
Affiliation:
Institute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic
S.G. Goto
Affiliation:
Graduate School of Science, Osaka City University, Osaka, Japan
*
*Author for correspondence Tel.: +420 387775231 Fax: +420 385310354 E-mail: rozsypal@entu.cas.cz
Get access Rights & Permissions [Opens in a new window]

Abstract

The bean bug (Riptortus pedestris) is a pest of soybeans and other legumes in Japan and other Asian countries. It enters a facultative adult diapause on exposure to short days. While photoperiodism and diapause are well understood in R. pedestris, knowledge of cold tolerance is very limited, as is information on the effect of diapause on cold tolerance. We examined the effect of photoperiod, cold acclimation, and feeding status on cold tolerance in R. pedestris. We found that cold acclimation significantly increased survival at −10°C in both long- and short-day adult R. pedestris. Since the difference in cold survival between long- and short-day cold-acclimated groups was only marginal, we conclude that entering diapause is not crucial for R. pedestris to successfully pass through cold acclimation and become cold tolerant. We observed similar effects in 5th instar nymphs, with both long- and short-day cold-acclimated groups surviving longer cold exposures compared with non-acclimated groups. Starvation, which was tested only in adult bugs, had only a negligible and negative impact on cold survival. Although cold tolerance significantly increased with cold acclimation in adult bugs, supercooling capacity unexpectedly decreased. Our results suggest that changes in supercooling capacity as well as in water content are unrelated to cold tolerance in R. pedestris. An analysis of metabolites revealed differences between the treatments, and while several metabolites markedly increased with cold acclimation, their concentrations were too low to have a significant effect on cold tolerance.

Keywords

Riptortus pedestriscold acclimationcold tolerancediapause
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 4 , August 2018 , pp. 487 - 493
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Block, W. (2003) Water or ice?-the challenge for invertebrate cold survival. Science Progress 86, 77–101.CrossRefGoogle ScholarPubMed
Clark, M.S. & Worland, M.R. (2008) How insects survive the cold: molecular mechanisms – a review. Journal of Comparative Physiology B 178, 917–933.CrossRefGoogle ScholarPubMed
Clegg, J.S., Seitz, P., Seitz, W. & Hazlewood, C.F. (1982) Cellular responses to extreme water loss: the water-replacement hypothesis. Cryobiology 19, 306–316.CrossRefGoogle ScholarPubMed
Danks, H.V. (2000) Dehydration in dormant insects. Journal of Insect Physiology 46, 837–852.CrossRefGoogle ScholarPubMed
Denlinger, D.L. (1991) Relationship between cold hardiness and diapause. pp. 174–198 in Lee, R.E. Jr & Denlinger, D.L. (Eds) Insects at Low Temperature. New York, Chapman and Hall.CrossRefGoogle Scholar
Des Marteaux, L.E. & Sinclair, B.J. (2016) Ion and water balance in Gryllus crickets during the first twelve hours of cold exposure. Journal of Insect Physiology 89, 19–27.Google Scholar
Doležal, P. & Sehnal, F. (2007) Effects of photoperiod and temperature on the development and diapause of the bark beetle Ips typographus. Journal of Applied Entomology 131, 165–173.Google Scholar
Fields, P.G. & McNeil, J.N. (1986) Possible dual cold-hardiness strategies in Cisseps fulvicollis Lepidoptera Arctiidae. Canadian Entomologist 118, 1309–1311.CrossRefGoogle Scholar
Gehrken, U., Strømme, A., Lundheim, R. & Zachariassen, K.E. (1991) Inoculative freezing in overwintering tenebrionid beetle, Bolitophagus reticulatus Panz. Journal of Insect Physiology 37, 683–687.Google Scholar
Hiiesaar, K., Williams, I., Luik, A., Metspalu, L., Muljar, R., Jõgar, K., Karise, R., Mänd, M., Svilponis, E. & Ploomi, A. (2009) Factors affecting cold hardiness in the small striped flea beetle, Phyllotreta undulata. Entomologia Experimentalis et Applicata 131, 278–285.Google Scholar
Hodková, M. & Hodek, I. (2004) Photoperiod, diapause and cold-hardiness. European Journal of Entomology 101, 445–458.Google Scholar
Ikeno, T., Tanaka, S.I., Numata, H. & Goto, S.G. (2010) Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biology 8, 116.Google Scholar
Khodayari, S., Moharramipour, S., Kamali, K., Javaran, M.J. & Renault, D. (2012) Effects of acclimation and diapause on the thermal tolerance of the two-spotted spider mite Tetranychus urticae. Journal of Thermal Biology 37, 419–423.CrossRefGoogle Scholar
Klepsatel, P., Gáliková, M., Xu, Y. & Kühnlein, R.P. (2016) Thermal stress depletes energy reserves in Drosophila. Scientific Reports 6, 33667.CrossRefGoogle ScholarPubMed
Košťál, V. (1993) Cold-hardiness and supercooling capacity in diapausing and nondiapausing stages of the cabbage root fly Delia radicum. Cryobiology 30, 524–531.CrossRefGoogle Scholar
Košťál, V. & Havelka, J. (2000) Diapausing larvae of the midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae) survive at subzero temperatures in a supercooled state but tolerate freezing if inoculated by external ice. European Journal of Entomology 97, 433–436.CrossRefGoogle Scholar
Košťál, V., Korbelová, J., Rozsypal, J., Zahradníčková, H., Cimlová, J., Tomčala, A. & Šimek, P. (2011) Long-term cold acclimation extends survival time at 0°C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster. PLoS ONE 6, e25025.CrossRefGoogle ScholarPubMed
Li, Y., Gong, H. & Park, H. (2000) Biochemistry and physiology of overwintering in the mature larva of the pine needle gall midge, Thecodiplosis japonensis (Diptera: Cecidmyiidae) in Korea. Cryo-Letters 21, 149–156.Google Scholar
Lundheim, R. (2002) Physiological and ecological significance of biological ice nucleators. Philosophical transactions of the Royal Society of London, B 357, 937–943.Google Scholar
MacMillan, H.A., Andersen, J.L., Davies, S.A. & Overgaard, J. (2015) The capacity to maintain ion and water homeostasis underlies interspecific variation in Drosophila cold tolerance. Scientific Reports 5, 18607.Google Scholar
Milonas, P.G. & Savopoulou-Soultani, M. (1999) Cold hardiness in diapause and non-diapause larvae of the summer fruit tortrix, Adoxophyes orana (Lepidoptera: Tortricidae). European Journal of Entomology 96, 183–187.Google Scholar
Moriya, S. (2005) Searching for overwintering sites of Riptortus clavatus (Thunberg) and Piezodorus hybneri (Gmelin) by re-analyzing litter samples originally collected at coppice forest floors for other kinds of stink bugs to estimate their overwintering densities. Annual Report of the Kanto-Tosan Plant Protection Society 52, 73–76.Google Scholar
Nakamura, K. & Numata, H. (2000) Photoperiodic control of the intensity of diapause and diapause development in the bean bug, Riptortus clavatus (Heteroptera: Alydidae). European Journal of Entomology 97, 19–23.CrossRefGoogle Scholar
Numata, H. & Hidaka, T. (1983) Photoperiodic control of adult diapause in the bean bug, Riptortus clavatus Thunberg (Heteroptera: Coreidae) II. Termination of diapause induced under different photoperiods. Applied Entomology and Zoology 18, 439–441.Google Scholar
Omura, S., Numata, H., & Goto, S.G. (2016) Circadian clock regulates photoperiodic responses governed by distinct output pathways in the bean bug, Riptortus pedestris. Biological Rhythm Research 47, 937–945.Google Scholar
Panizzi, A.R., Schaefer, C.W. & Natuhara, Y. (2000) Broad-headed bugs (Alydidae). pp. 321–336 in Schaefer, C.W. & Panizzi, A.R. (Eds) Heteroptera of Economic Importance. Boca Raton, CRC Press.Google Scholar
Ramløv, H. (2000) Aspects of natural cold tolerance in ectothermic animals. Human Reproduction 15, 26–46.Google Scholar
Rojas, R.R., Riemann, J.G. & Leopold, R.A. (1989) Diapause and overwintering capabilities of the larva of Homoeosoma electellum (Lepidoptera: Pyralidae). Environmental Entomology 18, 552–557.Google Scholar
Rozsypal, J., Košťál, V., Zahradníčková, H. & Šimek, P. (2013) Overwintering strategy and mechanisms of cold tolerance in the codling moth (Cydia pomonella). PLoS ONE 8, e61745.Google Scholar
Šlachta, M., Berková, P., Vambera, J. & Košťál, V. (2002) Physiology of the cold acclimation in non-diapasusing adults of Pyrrhocorisapterus (Heteroptera). European Journal of Entomology 99, 181–187.Google Scholar
Sømme, L. (1999) The physiology of cold hardiness in terrestrial arthropods. European Journal of Entomology 96, 1–10.Google Scholar
Sømme, L. & Block, W. (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38, 168–176.Google Scholar
Storey, K.B. & Storey, J.M. (1991) Biochemistry of cryoprotectants. pp. 64–93 in Lee, R.E. Jr & Denlinger, D.L. (Eds) Insects at Low Temperature. New York, Chapman and Hall.Google Scholar
Storey, K.B., Wilkie, D.R., Cairns, A., Thomas, H., Cowan, D.A., Baust, J., Pullin, A.S., Russell, N.J., & Jaenicke, R. (1990) Biochemical adaptation for cold hardiness in insects [and discussion]. Philosophical Transactions of the Royal Society of London B 326, 635–654.Google Scholar
Ter Braak, C.J.F. & Šmilauer, P. (2012) Canoco Reference Manual and User's Guide: Software for Ordination, version 5.0. 496 pp. Microcomputer Power, Ithaca, USA.Google Scholar
Timasheff, S.N. (2002) Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proceedings of the National Academy of Sciences 99, 9721–9726.CrossRefGoogle ScholarPubMed
Vesterlund, S.R., Lilley, T.M., van Ooik, T. & Sorvari, J. (2014) The effect of overwintering temperature on the body energy reserves and phenoloxidase activity of bumblebee Bombus lucorum queens. Insectes Sociaux 61, 265–272.CrossRefGoogle Scholar
Wilson, P.W., Heneghan, A.F. & Haymet, A.D.J. (2003) Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46, 88–98.Google Scholar
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.Google Scholar
Yoder, J.A., Benoit, J.B., Denlinger, D.L. & Rivers, D.B. (2006) Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. Journal of Insect Physiology 52, 202–214.Google Scholar
Supplementary material: PDF

Rozsypal et al supplementary material 1

Rozsypal et al supplementary material

Download Rozsypal et al supplementary material 1(PDF)
PDF 540.4 KB
Supplementary material: File

Rozsypal et al supplementary material 2

Rozsypal et al supplementary material

Download Rozsypal et al supplementary material 2(File)
File 28.1 KB