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      Effects of the winter temperature regime on survival, body mass loss and post-winter starvation resistance in laboratory-reared and field-collected ladybirds

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      Scientific Reports
      Nature Publishing Group UK
      Invasive species, Ecophysiology

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          Abstract

          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.

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          Insect overwintering in a changing climate.

          Insects are highly successful animals inhabiting marine, freshwater and terrestrial habitats from the equator to the poles. As a group, insects have limited ability to regulate their body temperature and have thus required a range of strategies to support life in thermally stressful environments, including behavioural avoidance through migration and seasonal changes in cold tolerance. With respect to overwintering strategies, insects have traditionally been divided into two main groups: freeze tolerant and freeze avoiding, although this simple classification is underpinned by a complex of interacting processes, i.e. synthesis of ice nucleating agents, cryoprotectants, antifreeze proteins and changes in membrane lipid composition. Also, in temperate and colder climates, the overwintering ability of many species is closely linked to the diapause state, which often increases cold tolerance ahead of temperature-induced seasonal acclimatisation. Importantly, even though most species can invoke one or both of these responses, the majority of insects die from the effects of cold rather than freezing. Most studies on the effects of a changing climate on insects have focused on processes that occur predominantly in summer (development, reproduction) and on changes in distributions rather than winter survival per se. For species that routinely experience cold stress, a general hypothesis would be that predicted temperature increases of 1 degree C to 5 degrees C over the next 50-100 years would increase winter survival in some climatic zones. However, this is unlikely to be a universal effect. Negative impacts may occur if climate warming leads to a reduction or loss of winter snow cover in polar and sub-polar areas, resulting in exposure to more severe air temperatures, increasing frequency of freeze-thaw cycles and risks of ice encasement. Likewise, whilst the dominant diapause-inducing cue (photoperiod) will be unaffected by global climate change, higher temperatures may modify normal rates of development, leading to a decoupling of synchrony between diapause-sensitive life-cycle stages and critical photoperiods for diapause induction. In terms of climate warming and potential heat stress, the most recent predictions of summer temperatures in Europe of 40 degrees C or higher in 50-75 years, are close to the current upper lethal limit of some insects. Long-term data sets on insect distributions and the timing of annual migrations provide strong evidence for 'positive' responses to higher winter temperatures over timescales of the past 20-50 years in North America, Europe and Asia.
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            Cold truths: how winter drives responses of terrestrial organisms to climate change.

            Winter is a key driver of individual performance, community composition, and ecological interactions in terrestrial habitats. Although climate change research tends to focus on performance in the growing season, climate change is also modifying winter conditions rapidly. Changes to winter temperatures, the variability of winter conditions, and winter snow cover can interact to induce cold injury, alter energy and water balance, advance or retard phenology, and modify community interactions. Species vary in their susceptibility to these winter drivers, hampering efforts to predict biological responses to climate change. Existing frameworks for predicting the impacts of climate change do not incorporate the complexity of organismal responses to winter. Here, we synthesise organismal responses to winter climate change, and use this synthesis to build a framework to predict exposure and sensitivity to negative impacts. This framework can be used to estimate the vulnerability of species to winter climate change. We describe the importance of relationships between winter conditions and performance during the growing season in determining fitness, and demonstrate how summer and winter processes are linked. Incorporating winter into current models will require concerted effort from theoreticians and empiricists, and the expansion of current growing-season studies to incorporate winter.
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              Insects in fluctuating thermal environments.

              All climate change scenarios predict an increase in both global temperature means and the magnitude of seasonal and diel temperature variation. The nonlinear relationship between temperature and biological processes means that fluctuating temperatures lead to physiological, life history, and ecological consequences for ectothermic insects that diverge from those predicted from constant temperatures. Fluctuating temperatures that remain within permissive temperature ranges generally improve performance. By contrast, those which extend to stressful temperatures may have either positive impacts, allowing repair of damage accrued during exposure to thermal extremes, or negative impacts from cumulative damage during successive exposures. We discuss the mechanisms underlying these differing effects. Fluctuating temperatures could be used to enhance or weaken insects in applied rearing programs, and any prediction of insect performance in the field-including models of climate change or population performance-must account for the effect of fluctuating temperatures.
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                Author and article information

                Contributors
                knapp@fzp.czu.cz
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                18 March 2020
                18 March 2020
                2020
                : 10
                : 4970
                Affiliations
                ISNI 0000 0001 2238 631X, GRID grid.15866.3c, Department of Ecology, , Faculty of Environmental Sciences, Czech University of Life Sciences Prague, ; Kamýcká 129, Prague, Suchdol 165 00 Czech Republic
                Author information
                https://orcid.org/http://orcid.org/0000-0003-4487-7317
                Article
                61820
                10.1038/s41598-020-61820-7
                7080747
                32188924
                4faca734-650b-4b44-9c55-b753be46edc3
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 31 May 2019
                : 18 February 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100006206, Česká Zemědělská Univerzita v Praze (Czech University of Life Sciences Prague);
                Award ID: 42110/1312/3145
                Award ID: 42110/1312/3145
                Award Recipient :
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                © The Author(s) 2020

                Uncategorized
                invasive species,ecophysiology
                Uncategorized
                invasive species, ecophysiology

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