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

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 laboratoryreared 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 laboratoryreared and field-collected individuals indicate that quantitative conclusions derived from studies investigating solely laboratory-reared individuals cannot be directly extrapolated to field situations. An increasing body of literature shows that temperature is one of the most important factors determining the distribution of organisms on the globe 1-3. Also the distribution of insect species is strongly affected by temperature, and this relationship is especially apparent for winter temperatures 4,5. Overwintering insects have to overcome stressful environmental conditions, e.g., unavailable food resources, low temperatures or water deficits, and thus, it is unsurprising that many insect species suffer from substantial mortality during the winter period 5. In response, insects have adopted complex strategies to overcome stressful winter conditions 6,7. The low temperatures experienced during overwintering can result in the mortality of insects due to severe tissue damage caused by ice crystallization within cells or due to accumulated chill injuries resulting in metabolic disruptions, even at non-freezing temperatures 7. In general, insects may adopt one of two strategies to mitigate the danger of internal ice formation: either tolerate freezing (i.e., withstand the formation of ice) or avoid freezing (i.e., reduce the freezing point to a...

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

“…Note that high winter mortality of laboratory-reared beetles resulted in a limited number of individuals sampled in the last period, that is, after overwintering, especially for the cold winter treatment (n warm = 36, n average = 33, n cold = 12; see our dataset in Supporting Information Table S3). In our previous study (Knapp and Řeřicha 2020), we showed that winter survival was significantly lower for laboratory-reared compare to field-collected ladybirds. We suppose that environmental stability experienced during ladybird development or food quality, for example, Ephestia egg diet can limit ladybird capacity to produce cryoprotectants, may be responsible for this pattern.…”

“…Unfortunately, a low number of experimental studies investigating the effects of winter period on immune responses do not allow us to make generalizations that lead to particular patterns. As temperate insects are facing a limited energy budget during overwintering (Ferguson et al 2018a, Knapp andŘeřicha 2020), decreasing haemocyte concentrations through the winter could be linked to the high energetic costs of cellular immunity maintenance compared to humoral immunity (Ferguson et al 2016). Note that stress in the form of limited energy sources caused by starvation, results in a reduced haemocyte F I G U R E 3 Sex-specific effects of overwintering on total protein concentration in the field-collected Harmonia axyridis ladybirds.…”

“…Change in antimicrobial activity against E. coli from autumn to spring is presented separately for naïve ladybirds (gray line) and beetles challenged by E. coli injection 24 hours prior to measurement (black line). Means ± SEM are shown concentration also during growing season in H. axyridis (Knapp and Řeřicha 2020). An interpretation of changes in the immune system parameters during winter is complicated by the fact that insects during overwintering have to integrate physiological responses to multiple stressors, for example, low temperature, desiccation, pathogens, and limited energy reserves, that can interact with each other (Ferguson et al 2016, Ferguson andSinclair 2017).…”

“…This pattern can be explained by increased expression of genes responsible for the production of antimicrobial peptides following an immune challenge (Schmidtberg et al 2013). As induced immune response increases energy expenditure (Adamo et al 2016), a possible explanation for the low inducibility of the immune system after overwintering is limited energy budget at this stage (the energetic reserves of H. axyridis are very low at the end of overwintering period; Knapp and Řeřicha 2020;M. Řeřicha unpublished data).…”

“…The overwintering part of Experiment 1 started on October 15, 2015. The beetles were exposed to three winter temperature regimes: 1) warm winter, 2) average winter and 3) cold winter, using computer-controlled climatic chambers (see Knapp and Řeřicha 2020, for details). The temperature was adjusted every hour with a new temperature to mimic real temperatures experienced by H. axyridis in outdoor shelters in Central Europe (the temperatures applied are attached as Supporting Information file Table S2).…”