Ongoing climate change results in increasing temperatures throughout the seasons. The effects of climate change on insect performance are less studied during the winter season than during the growing season. Here, we investigated the effects of various winter temperature regimes (warm, normal and cold) on the winter performance of the invasive ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Winter survival, body mass loss and post-winter starvation resistance were measured for a laboratory-reared population as well as three populations collected from the field prior to overwintering. The warm winter regime increased the survival rate and body mass loss and reduced post-winter starvation resistance compared to those of the ladybirds in the cold winter regime. The effects of the temperature regime were qualitatively similar for the laboratory-reared and field-collected beetles; however, there were significant quantitative differences in all measured overwintering parameters between the laboratory-reared and field-collected populations. The winter survival of the laboratory-reared beetles was much lower than that of the field-collected beetles. The laboratory-reared beetles also lost a larger proportion of their body mass and had reduced post-winter starvation resistance. Winter survival was similar between the females and males, but compared to the males, the females lost a smaller proportion of their body mass and had better post-winter starvation resistance. The pre-overwintering body mass positively affected winter survival and post-winter starvation resistance in both the laboratory-reared and field-collected ladybirds. The significant differences between the laboratory-reared and field-collected individuals indicate that quantitative conclusions derived from studies investigating solely laboratory-reared individuals cannot be directly extrapolated to field situations.

Department of Ecology Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcká 129 Prague Suchdol 165 00 Czech Republic

Zobrazit více v PubMed

Araujo MB, et al. Quaternary climate changes explain diversity among reptiles and amphibians. Ecography. 2008;31:8–15. doi: 10.1111/j.2007.0906-7590.05318.x. DOI

Morgan ER, Jefferies R, Krajewski M, Ward P, Shaw SE. Canine pulmonary angiostrongylosis: The influence of climate on parasite distribution. Parasitology International. 2009;58:406–410. doi: 10.1016/j.parint.2009.08.003. PubMed DOI

Szentivanyi T, et al. Climatic effects on the distribution of ant- and bat fly-associated fungal ectoparasites (Ascomycota, Laboulbeniales) Fungal Ecology. 2019;39:371–379. doi: 10.1016/j.funeco.2019.03.003. DOI

Bale JS, Hayward SAL. Insect overwintering in a changing climate. Journal of Experimental Biology. 2010;213:980–994. doi: 10.1242/jeb.037911. PubMed DOI

Williams CM, Henry HAL, Sinclair BJ. Cold truths: How winter drives responses of terrestrial organisms to climate change. Biological Reviews. 2015;90:214–235. doi: 10.1111/brv.12105. PubMed DOI

Hahn DA, Denlinger DL. Meeting the energetic demands of insect diapause: Nutrient storage and utilization. Journal of Insect Physiology. 2007;53:760–773. doi: 10.1016/j.jinsphys.2007.03.018. PubMed DOI

Turnock WJ, Fields PG. Winter climates and coldhardiness in terrestrial insects. European Journal of Entomology. 2005;102:561–576. doi: 10.14411/eje.2005.081. DOI

Sinclair BJ, Addo-Bediako A, Chown SL. Climatic variability and the evolution of insect freeze tolerance. Biological Reviews of the Cambridge Philosophical Society. 2003;78:181–195. doi: 10.1017/S1464793102006024. PubMed DOI

Toxopeus J, Sinclair BJ. Mechanisms underlying insect freeze tolerance. Biological Reviews. 2018;93:1891–1914. doi: 10.1111/brv.12425. PubMed DOI

Duman JG. Antifreeze and Ice Nucleator Proteins in Terrestrial Arthropods. Annual Review of Physiology. 2001;63:327–357. doi: 10.1146/annurev.physiol.63.1.327. PubMed DOI

Sinclair BJ, Vernon P, Klok CJ, Chown SL. Insects at low temperatures: An ecological perspective. Trends in Ecology and Evolution. 2003;18:257–262. doi: 10.1016/S0169-5347(03)00014-4. DOI

Watanabe M. Cold tolerance and myo-inositol accumulation in overwintering adults of a lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae) European Journal of Entomology. 2002;99:5–9. doi: 10.14411/eje.2002.002. DOI

Knapp M, Vernon P, Renault D. Studies on chill coma recovery in the ladybird, Harmonia axyridis: Ontogenetic profile, effect of repeated cold exposures, and capacity to predict winter survival. Journal of Thermal Biology. 2018;74:275–280. doi: 10.1016/j.jtherbio.2018.04.013. PubMed DOI

Overgaard J, MacMillan HA. The Integrative Physiology of Insect Chill Tolerance. Annual Review of Physiology. 2017;79:187–208. doi: 10.1146/annurev-physiol-022516-034142. PubMed DOI

Hahn DA, Denlinger DL. Energetics of Insect Diapause. Annual Review of Entomology. 2011;56:103–121. doi: 10.1146/annurev-ento-112408-085436. PubMed DOI

Tauber, M. J., Tauber, C. A. & Masaki, S. Seasonal adaptations of insects. (Oxford University Press, 1986).

Koštál V. Eco-physiological phases of insect diapause. Journal of Insect Physiology. 2006;52:113–127. doi: 10.1016/j.jinsphys.2005.09.008. PubMed DOI

Irwin JT, Lee RE. Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos. 2003;100:71–78. doi: 10.1034/j.1600-0706.2003.11738.x. DOI

Sinclair BJ. Linking energetics and overwintering in temperate insects. Journal of Thermal Biology. 2015;54:5–11. doi: 10.1016/j.jtherbio.2014.07.007. PubMed DOI

Musolin DL, Tougou D, Fujisaki K. Too hot to handle? Phenological and life-history responses to simulated climate change of the southern green stink bug Nezara viridula (Heteroptera: Pentatomidae) Global Change Biology. 2010;16:73–87. doi: 10.1111/j.1365-2486.2009.01914.x. DOI

Dalton DT, et al. Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Management Science. 2011;67:1368–1374. doi: 10.1002/ps.2280. PubMed DOI

Taylor CM, Coffey PL, Hamby KA, Dively GP. Laboratory rearing of Halyomorpha halys: methods to optimize survival and fitness of adults during and after diapause. Journal of Pest Science. 2017;90:1069–1077. doi: 10.1007/s10340-017-0881-9. DOI

Bosch J, Kemp WP. Effect of Wintering Duration and Temperature on Survival and Emergence Time in Males of the Orchard Pollinator Osmia lignaria (Hymenoptera: Megachilidae) Environmental Entomology. 2003;32:711–716. doi: 10.1603/0046-225X-32.4.711. DOI

Stuhldreher G, Hermann G, Fartmann T. Cold-adapted species in a warming world - an explorative study on the impact of high winter temperatures on a continental butterfly. Entomologia Experimentalis et Applicata. 2014;151:270–279. doi: 10.1111/eea.12193. DOI

Xiao H, Chen J, Chen L, Chen C, Wu S. Exposure to mild temperatures decreases overwintering larval survival and post-diapause reproductive potential in the rice stem borer Chilo suppressalis (J Pest Sci, 10.1007/s10340-016-0769-0) Journal of Pest Science. 2017;90:127. doi: 10.1007/s10340-016-0799-7. DOI

Aukema BH, et al. Movement of outbreak populations of mountain pine beetle: Influences of spatiotemporal patterns and climate. Ecography. 2008;31:348–358. doi: 10.1111/j.0906-7590.2007.05453.x. DOI

Caminade C, et al. Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. Journal of The Royal Society Interface. 2012;9:2708–2717. doi: 10.1098/rsif.2012.0138. PubMed DOI PMC

Enriquez T, Ruel D, Charrier M, Colinet H. Effects of fluctuating thermal regimes on cold survival and life history traits of the spotted wing Drosophila (Drosophila suzukii) Insect Science. 2020;27:317–335. doi: 10.1111/1744-7917.12649. PubMed DOI

Xing K, Hoffmann AA, Zhao F, Ma CS. Wide diurnal temperature variation inhibits larval development and adult reproduction in the diamondback moth. Journal of Thermal Biology. 2019;84:8–15. doi: 10.1016/j.jtherbio.2019.05.013. PubMed DOI

Colinet H, Sinclair BJ, Vernon P, Renault D. Insects in Fluctuating Thermal Environments. Annual Review of Entomology. 2015;60:123–140. doi: 10.1146/annurev-ento-010814-021017. PubMed DOI

Berkvens N, Bale JS, Berkvens D, Tirry L, De Clercq P. Cold tolerance of the harlequin ladybird Harmonia axyridis in Europe. Journal of Insect Physiology. 2010;56:438–444. doi: 10.1016/j.jinsphys.2009.11.019. PubMed DOI

Brown PMJ, et al. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, dispersal and routes of invasion. BioControl. 2011;56:623–641. doi: 10.1007/s10526-011-9379-1. DOI

Lombaert E, et al. Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: Case study of the invasive ladybird Harmonia axyridis. Molecular Ecology. 2011;20:4654–4670. doi: 10.1111/j.1365-294X.2011.05322.x. PubMed DOI

Brown PMJ, et al. Harmonia axyridis in Europe: Spread and distribution of a non-native coccinellid. BioControl. 2008;53:5–21. doi: 10.1007/978-1-4020-6939-0_2. DOI

Roy HE, et al. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biological Invasions. 2016;18:997–1044. doi: 10.1007/s10530-016-1077-6. DOI

Camacho-Cervantes, M., Ortega-Iturriaga, A. & Del-Val, E. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. Peerj5, 10.7717/peerj.3296 (2017). PubMed PMC

Hiller T, Haelewaters D. A case of silent invasion: Citizen science confirms the presence of Harmonia axyridis (Coleoptera, Coccinellidae) in Central America. Plos One. 2019;14:e0220082. doi: 10.1371/journal.pone.0220082. PubMed DOI PMC

Ukrainsky AS, Orlova-Bienkowskaja MJ. Expansion of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) to European Russia and adjacent regions. Biological Invasions. 2014;16:1003–1008. doi: 10.1007/s10530-013-0571-3. DOI

Barahona-Segovia RM, Grez AA, Bozinovic F. Testing the hypothesis of greater eurythermality in invasive than in native ladybird species: From physiological performance to life-history strategies. Ecological Entomology. 2016;41:182–191. doi: 10.1111/een.12287. DOI

Grez AA, Zaviezo T, Roy HE, Brown PMJ, Segura B. In the shadow of the condor: invasive Harmonia axyridis found at very high altitude in the Chilean Andes. Insect Conservation and Diversity. 2017;10:483–487. doi: 10.1111/icad.12258. DOI

Danks, H. V. Insect Dormancy: An Ecological Perspective. Biological Survey of Canada (Terrestrial Arthropods), 433 (1987).

Hodek, I., van Emden, H. F. & Honěk, A. Ecology and Behaviour of the Ladybird beetles (Coccinellidae). 561 (2012).

Labrie G, Coderre D, Lucas E. Overwintering Strategy of Multicolored Asian Lady Beetle (Coleoptera: Coccinellidae): Cold-Free Space as a Factor of Invasive Success. Annals of the Entomological Society of America. 2008;101:860–866. doi: 10.1093/aesa/101.5.860. DOI

Raak-Van Den Berg CL, De Jong PW, Hemerik L, Van Lenteren JC. Diapause and post-diapause quiescence demonstrated in overwintering Harmonia axyridis (Coleoptera: Coccinellidae) in northwestern Europe. European Journal of Entomology. 2013;110:585–591. doi: 10.14411/eje.2013.079. DOI

Reznik SY, Dolgovskaya MY, Ovchinnikov AN, Belyakova NA. Weak photoperiodic response facilitates the biological invasion of the harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) Journal of Applied Entomology. 2015;139:241–249. doi: 10.1111/jen.12158. DOI

Falt-Nardmann JJJ, et al. The recent northward expansion of Lymantria monacha in relation to realised changes in temperatures of different seasons. Forest Ecology and Management. 2018;427:96–105. doi: 10.1016/j.foreco.2018.05.053. DOI

Sinclair BJ, Marshall KE. The many roles of fats in overwintering insects. The Journal of Experimental Biology. 2018;221:jeb161836. doi: 10.1242/jeb.161836. PubMed DOI

Lidwien Raak-van den Berg C, Stam JM, De Jong PW, Hemerik L, van Lenteren JC. Winter survival of Harmonia axyridis in The Netherlands. Biological Control. 2012;60:68–76. doi: 10.1016/j.biocontrol.2011.10.001. DOI

Yang X-B, Zhang Y-M, Henne DC, Liu T-X. Life Tables of Bactericera cockerelli (Hemiptera: Triozidae) on Tomato Under Laboratory and Field Conditions in Southern Texas. Florida Entomologist. 2013;96:904–913. doi: 10.1653/024.096.0326. DOI

Řeřicha M, Dobeš P, Hyršl P, Knapp M. Ontogeny of protein concentration, haemocyte concentration and antimicrobial activity against Escherichia coli in haemolymph of the invasive harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) Physiological Entomology. 2018;43:51–59. doi: 10.1111/phen.12224. DOI

Knapp M, Nedvěd O. Gender and Timing during Ontogeny Matter: Effects of a Temporary High Temperature on Survival, Body Size and Colouration in Harmonia axyridis. PLoS ONE. 2013;8:e74984. doi: 10.1371/journal.pone.0074984. PubMed DOI PMC

Aggarwal DD. Physiological basis of starvation resistance in Drosophila leontia: analysis of sexual dimorphism. Journal of Experimental Biology. 2014;217:1849–1859. doi: 10.1242/jeb.096792. PubMed DOI

Knapp M. Relative importance of sex, pre-starvation body mass and structural body size in the determination of exceptional starvation resistance of Anchomenus dorsalis (Coleoptera: Carabidae) PLoS ONE. 2016;11:e151459. doi: 10.1371/journal.pone.0151459. PubMed DOI PMC

Knapp M, Knappova J. Measurement of body condition in a common carabid beetle, Poecilus cupreus: a comparison of fresh weight, dry weight, and fat content. Journal of Insect Science. 2013;13(article):6. doi: 10.1673/031.013.0601. PubMed DOI PMC

Gergs A, Jager T. Body size-mediated starvation resistance in an insect predator. Journal of Animal Ecology. 2014;83:758–768. doi: 10.1111/1365-2656.12195. PubMed DOI

Kovacs JL, Goodisman MAD. Effects of Size, Shape, Genotype, and Mating Status on Queen Overwintering Survival in the Social Wasp Vespula maculifrons. Environmental Entomology. 2012;41:1612–1620. doi: 10.1603/en12023. PubMed DOI

Sgolastra F, et al. The long summer: Pre-wintering temperatures affect metabolic expenditure and winter survival in a solitary bee. Journal of Insect Physiology. 2011;57:1651–1659. doi: 10.1016/j.jinsphys.2011.08.017. PubMed DOI

Therneau, T. M. Package ‘coxme’: Mixed Effects Cox Models, version 2.2-10. (2018).

R Development Core Team. A language and environment for statistical computing. Available at http://www.R-project.org, (2018).

Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biometrical Journal. 2008;50:346–363. doi: 10.1002/bimj.200810425. PubMed DOI

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Team, R. D. C. Nlme: linear and nonlinear mixed effects models. R package version 3.1-107. Available at https://cran.r-project.org/web/packages/nlme/nlme.pdf, (2018).

Ripley, B. et al. Package ‘MASS’, version 7.3-50. (2018).

Increased pupal temperature has reversible effects on thermal performance and irreversible effects on immune system and fecundity in adult ladybirds

Fungal ectoparasites increase winter mortality of ladybird hosts despite limited effects on their immune system

Changes in haemolymph parameters and insect ability to respond to immune challenge during overwintering