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

Abstract

Winter represents a challenging period for insects inhabiting temperate regions. A plethora of studies have investigated how environmental conditions such as temperature affect insect overwintering success. However, only a few studies have focused on biotic factors and the mechanisms affecting the overwintering performance of insects. Here, we investigated the effects of the parasitic fungus Hesperomyces virescens on the overwintering performance and immune system functioning of the invasive ladybird Harmonia axyridis. Winter survival was significantly lower for infected than for uninfected ladybirds. Body mass loss during overwintering tends to be higher for infected individuals compared to uninfected ones and for larger ladybirds. In addition, parasitic infection reduced post-winter longevity without food in male but not female ladybirds. Total haemocyte and protein concentration as well as antimicrobial activity against Escherichia coli significantly decreased during ladybird overwintering. However, haemolymph parameters were only poorly affected by Hesperomyces infection, with the exception of antimicrobial activity against E. coli that tended to be higher in infected ladybirds. Interestingly, none of the pre-winter haemolymph parameters were good predictors of ladybird winter survival. Overall, our results indicate that energy exhaustion unrelated to immune system challenge is the most probable explanation for increased overwintering mortality in infected ladybirds.

Keywords: body condition; ecophysiology; microsporidia load; pathogen; sexually transmitted diseases; stress resistance.

Figure 1.

Effects of fungal infection on (a) winter survival (n = 207) and (b) post-winter longevity (n = 92), and interactive effects of fungal infection and sex on (c) post-winter body mass change (n= 93) of Harmonia axyridis. For each response variable, the estimates and 95% CI from the models and the raw data for uninfected (green dots) and heavily infected beetles (red dots) are shown. Black dots and stars indicate statistical significance (· = p < 0.1; * = p < 0.05; *** = p < 0.001). (Online version in colour.)

Figure 2.

Effects of fungal infection and season on (a) antimicrobial activity (n = 94, (b) haemocytes (n = 102), (c) proteins (n = 102) and (d) microsporidia (n = 102) in Harmonia axyridis haemolymph. For each response variable, mean ± s.e. and raw data are shown for uninfected (green dots) and heavily infected beetles (red dots). Note that the number of microsporidia only represents relative values (for further details, see §2). Black dots and stars indicate statistical significance (n.s. = not significant; · = p < 0.1; *** = p < 0.001). n values represent the complete number of observations, i.e. total number of samples analysed in both autumn and spring. (Online version in colour.)

Figure 3.

Correlations between pre-overwintering haemolymph parameters. The lower triangle shows scatterplots for each pair of variables, and the upper triangle, the Pearson correlation indices. Stars indicate the significance of correlations (***: p < 0.001; *: p < 0.05), and numbers represent r values. The diagonal panels represent density distributions plots for each variable. (Online version in colour.)