Cold adaptation strategies in lab-reared European grapevine moth Lobesia botrana: Exploring diapause induction, supercooling point, and cold hardiness

Pirmoradi Amozegarfard, Neda; Mikani, Azam; Mehrabadi, Mohammad; Moharramipour, Saeid

doi:10.48311/jcp.2023.1639

Cold adaptation strategies in lab-reared European grapevine moth Lobesia botrana: Exploring diapause induction, supercooling point, and cold hardiness

https://doi.org/10.48311/jcp.2023.1639

Volume 12, Issue 3
September 2023

Pages 283-297

Document Type : Original Research

Authors

N. Pirmoradi Amozegarfard

A. Mikani

M. Mehrabadi

S. Moharramipour

Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran.

Abstract

The European grapevine moth, Lobesia botrana (Denis and Schiffermueller) (Lepidoptera: Tortricidae), is a significant pest causing economic damage to vineyards worldwide. In this research, the cold tolerance of the pupae and its relationship with diapause was investigated at 23 ± 0.5 °C, 70 ± 5% RH, and LD 12:12 h. One-day-old eggs were transferred to LD 12:12 h to induce diapause at the pupal stage. Diapausing pupae exhibited a mean supercooling point (SCP) of -24.35 °C, whereas in the non-diapausing pupae (23 ± 0.5 °C, 70 ± 5% RH, LD 16:8 h), it was -23.06 °C, with no significant difference between the two groups. Furthermore, diapausing pupae demonstrated significantly higher cold tolerance (LT₅₀ of -14.43 °C) than non-diapausing pupae (LT₅₀ of -3.33 °C). Diapausing pupae tolerated subzero temperatures without significant changes in the SCP, tolerating 11 °C lower than control pupae due to the short daylength alone. Our results suggest that the diapause state and cold hardiness of L. botrana are independent of changes after SCP, and the insect employs a freeze-intolerant strategy to overcome subzero temperatures. Cold acclimation at -5 and -10 °C for 72 h induced a significant decrease in the SCP of diapausing pupae, while a 72-h cold acclimation had no notable impact on the SCP of non-diapausing pupae. These findings provide valuable insights into the survival mechanisms of the European grapevine moth under cold conditions and diapause-related adaptations.

Keywords

European grapevine moth

diapause induction

cold hardiness

Supercooling point

Tolerance

20.1001.1.22519041.2023.12.3.5.7

Andreadis, S. and Athanassiou, C. G. 2017. A review of insect cold hardiness and its potential in stored product insect control. Crop Protection. . 91: 93-99.
Andreadis, S. S., Milonas, P. G. and Savopoulou-Soultani, M. 2005. Cold hardiness of diapausing and non-diapausing pupae of the European grapevine moth, Lobesia botrana. Entomologia Experimentalis et Applicata.117: 113–118.
Bale, J. S. 1996. Insect cold hardiness: a matter of life and death. European Journal of Entomology, 93: 369–382.
Butterson, A., Roe, A. D. and Marshall, K. E. 2021. Plasticity of cold hardiness in the eastern spruce budworm, Choristoneura fumiferana. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 259: 110998.
Danks, H. V. 1987. Insect dormancy: an ecological perspective. Biological Survey of Canada, 439 pp.
Delisle, J., Bernier-Cardou, M. and Labrecque, A. 2022. Cold tolerance and winter survival of seasonally-acclimatised second-instar larvae of the spruce budworm, Choristoneura fumiferana. Ecological Entomology. 47(4): 553-565.
Denlinger, D. L. 2002. Regulation of diapause. Annual Review of Entomology, 47(1): 93-122.
Denlinger, D. L. 2008. Why study diapause?. Entomological Research, 38(1):1-9.
Denlinger, D. L. 2009. Encyclopedia of Insects (Second Edition). Chapter 72. Diapause. Academic Press. pp.267-271. doi:10.1016/B978-0-12-374144-8.00081-3.
Denlinger, D. L. 2023. Insect diapause: from a rich history to an exciting future. Journal of Experimental Biology. 226. jeb245329. doi:10.1242/jeb.245329.
Goehring, L. and Oberhauser, K. 2002. Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus. Ecological Entomology. 27:674-685.
Gray, D. R ., Ravlin. F. W. and Braine J. A. 2001. Diapause in the gypsy moth: a model of inhibition and development. Journal of Insect Physiology. 47 (2): 173-184.
Hahn, D. A. and Denlinger, D. L. 2007. Meeting the energetic demands of insect diapause: nutrient storage and utilization. Journal of Insect Physiology, 53(8): 760-773.
Hemmati, C., Moharramipour, S. and Talebi A. A. 2017. Diapause induced by temperature and photoperiod affects fatty acid compositions and cold tolerance of Phthorimaea operculella (Lepidoptera: Gelechiidae). Environmental. Entomology. 46: 1456–1463.
Herman, W. S. 2002. Studies on the adult reproductive diapause of the monarch butterfly, Danaus plexippus. The Biological Bulletin. 160 (1): 89-106.
Hodek, I., Van Emden, H. F. and Honěk, A. 2012. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Chapter 6: Diapause/Dormancy.Wiley-Blackwell, Oxford, 275–342.
Ioriatti, C., Anfora, G., Bagnoli, B., Benelli, G. and Lucchi, A., 2023. A review of history and geographical distribution of grapevine moths in Italian vineyards in light of climate change: Looking backward to face the future. Crop Protection, p.106375.
Ioriatti, C., Anfora, G., Tasin, M., De Cristofaro, A., Witzgall, P., and Lucchi, A. 2011. Chemical ecology and management of Lobesia botrana (Lepidoptera: Tortricidae). Journal of Economic Entomology. 104(4): 1125–1137.
Ioriatti, C., Lucchi, A., & Varela, L. G. 2012. Grape berry moths in western European vineyards and their recent movement into the New World. In: Arthropod Management in Vineyards: Pests, Approaches, and Future Directions. Bostanian, N. J., Vincent, C. and Isaacs, R. (Eds.), Dordrecht: Springer, pp. 339–359. https:// doi.org/10.1007/978-94-007-4032-7_14.
Keosentse, O., Mutamiswa, R., Plessis, H. D. and Nyamukondiwa, C. 2021. Developmental stage variation in Spodoptera frugiperda (Lepidoptera: Noctuidae) low temperature tolerance: implications for overwintering. Austeral Entomology. 60 (2): 400-410.
Khani, A., and Moharramipour, S. 2010. Cold hardiness and supercooling capacity in the overwintering larvae of the codling moth, Cydia pomonella. Journal of Insect Science. 10: 83.
Kono, Y. 1970. Photoperiodic induction of diapause in Pieris rapae crucivora Boisduval (Lepidoptera: Pieridae). Applied Entomology and Zoology, 5 (4): 213-224.
Koštál, V. 2006. Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52(2): 113-127.
Koštál, V., Mollaei, M. and Schöttner, k. 2016. Diapause induction as an interplay between seasonal token stimuli, and modifying and directly limiting factors: hibernation in Chymomyza costata. Physiological Entomology.41: 344-357.
Leather, S. R. 1993. Overwintering in six arable aphid pests: a review with particular relevance to pest management. Jouranal of Applied Entomology. 116: 217-223.
Lee, R. E. 1991. Principles of insect low temperature tolerance. pp. 17–46. In R. E. Lee and D. L. Denlinger (eds.), Insects at low temperature. Chapman & Hall, New York.
Lee, R. E. 2010. A primer on insect cold-tolerance. In: Low Temperature Biology of Insects. Denlinger, D. L. and Lee, R. E. (Eds.), Cambridge, New York. pp. 15-34.
Lee, R. E., Costanzo, J. P. and Lee, M. R. 2019. Reducing cold-hardiness of insect pests using ice nucleating active microbes. In: Temperature Sensitivity in Insects and Application in Integrated Pest Management. Hallman, G. J. and Denlinger, D. L. (Eds.), e book, CRC Press. New York, NY, USA. pp. 97-124.
Li, N. G., Toxopeus, J., Moos, M., Sørensen, J. G. and Sinclair, B. J. 2020. A comparison of low temperature biology of Pieris rapae from Ontario, Canada, and Yakutia, Far Eastern Russia. Comparative Biochemistry and Physiology. Part A.doi: 10.1016/j.cbpa.2020.110649.
Mansingh, A. 1974. Studies in insect dormancy. II. Relationship of cold hardiness to diapause and quiescence in the eastern tent caterpillar, Malacosoma americanum (Fab.), (Lepidoptera: Lasiocampidae). Canadian Journal of Zoology. 52: 629–637.
Marshall, K. E. and Sinclair, B. J. 2011. The sub-lethal effects of repeated freezing in the woolly bear caterpillar Pyrrharctia isabella. Journal of Experimental Biology. 214 (7): 1205-1212.
Masoudmagham, A., Izadi, H, and Mohammadzadeh, M. 2021. Expanded Supercooling Capacity with No Cryoprotectant Accumulation Underlies Cold Tolerance of the European grapevine moth. Journal of Economic Entomology. 114(2), 828–838.
Pavan, F., Bigot, G., Cargnus, E. and Zandigiacomo, P. 2014. Influence of the carpophagous generations of the European grapevine moth Lobesia botrana on grape bunch rots. Phytoparasitica 42: 61–69.
Pavan, F., Floreani, C., Barro, P., Zandigiacomo, P. and Dalla Monta, L. 2013. Occurrence of two different development patterns in Lobesia botrana (Lepidoptera: Tortricidae) larvae during the second generation. Agricultural and Forest Entomology. 15: 398–406.
Rank, A., Ramos, R. S., Silva, R. S., Soares, J. R. S., Picanço, M. C. and Fidelis, E.G. 2020. Risk of the introduction of Lobesia botrana in suitable areas for Vitis vinifera. Journal of Pest Science. 93: 1167–1179.
Rapagnani, M. R., Caffarelli, V., Barlattani, M. and Minelli, F. 1990. Descrizione di un allevamento, in laboratorio, della tignoletta dell’uva Lobesia botrana Den. E Schiff. (Lepidoptera: Tortricidae) su un nuovo alimento semi-sintetico. Bulletin of Insectology. 44: 57–64.
Roach, S. H. and Adkisson, P. L. 1970. Rôle of photoperiod and temperature in the induction of pupal diapause in the bollworm, Heliothis zea. Journal of Insect Physiology. 16: 1591-1597.
Roditakis, N. E. and Karandinos, M. G. 2001. Effects of photoperiod and temperature on pupal diapause induction of grapevine moth Lobesia botrana. Physiological Entomology. 26: 329–340.
Rozsypal, J. and Koštál, V. Supercooling and freezing as eco-physiological alternatives rather than mutually exclusive strategies: A case study in Pyrrhocoris apterus. Journal of Insect Physiology. 111: 53-62.
Saeidi, F., Moharramipour, S. and Barzegar, M. 2012: Seasonal patterns of cold hardiness and cryoprotectant profiles in Brevicoryne brassicae (Hemiptera: Aphididae). Environmental Entomology. 41: 1638–1643.
Shimizu, I. 1982. Photoperiodic induction in the silkworm, Bombyx mori, reared on artificial diet: Evidence for extraretinal photoreception. Journal of Insect Physiology. 28 (10): 841-846.
Sinclair, B. J., L. E. Coello Alvarado, and L. V. Ferguson. 2015. An invitation to measure insect cold tolerance: Methods, approaches, and workflow. Journal of Thermal Biology. 53: 180–197.
Sinclair, B. J., Vernon, P., Klok, C. and Chown, S. 2003. Insects at low temperatures: an ecological perspective. Trends in Ecology & Evolution, 18(5): 257-262.
Štětina, T., Koštál, V. and Korbelová, J. 2015. The role of inducible hsp70, and other heat shock proteins, in adaptive complex of cold tolerance of the fruit fly (Drosophila melanogaster). PLOS ONE. doi:10.1371/journal.pone.0128976. [Accessed 2th January 2015].
Storey, K. B. and Storey, J. M. 2013. Molecular biology of freezing tolerance. Comparative Physiology, 3: 1283–1308.
Storey, K. B. and Storey, J. M. 1988. Freeze tolerance in animals. Physiological Reviews. 68: 27–84.
Tauber, M. J., Tauber, C. A., Ruberson, J. R., Tauber, A. J. and Abrahamson, L. P. 1990. Dormancy in Lymantria dispar (Lepidoptera: Lymantriidae): Analysis of Photoperiodic and Thermal Responses. Annals of the Entomological Society of America. 83 (3): 494-503.
Thiéry, D., Monceau, K. and Moreau, J. 2014. Larval intraspecific competition for food in the European grapevine moth Lobesia botrana. Bulletin of Entomological Research, 104 (4): 517-524.
Tobita, H. and Kiuchi ,T. 2022. Knockouts of positive and negative elements of the circadian clock disrupt photoperiodic diapause induction in the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology. 149: 103842.
Vatanparast, M. and Park,Y. 2022. Cold tolerance strategies of the fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Scientific Reports. 12: 4129.

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