Upper thermal limits differ among and within component species in a tritrophic host-parasitoid-hyperparasitoid system

Abstract

Understanding how climate change affects host-parasite systems and predicting the consequences for ecosystems, economies, and human health has emerged as an important task for science and society. Some basic insight into this complex problem can be gained by comparing the thermal physiology of interacting host and parasite species. In this study, we compared upper thermal tolerance among three component species in a natural host-parasitoid-hyperparasitoid system from Virginia, USA. To assess the ecological relevance of our results, we also examined a record of maximum daily air temperatures collected near the study site in the last 124 years. We found that the caterpillar host Manduca sexta had a critical thermal maximum (CTmax) about 4°C higher than the parasitic wasp, Cotesia congregata, and the hyperparasitic wasp, Conura sp., had a CTmax about 6°C higher than its host, C. congregata. We also found significant differences in CTmax among instars and between parasitized and non-parasitized M. sexta. The highest maximum daily air temperature recorded near the study in the last 124 years was 42°C, which equals the average CTmax of one species (C. congregata) but is several degrees lower than the average CTmax of the other two species (M. sexta, Conura sp.) in this study. Our results combined with other studies suggest that significant differences in thermal performance within and among interacting host and parasite species are common in nature and that climate change may be largely disruptive to these systems with responses that are highly variable and complex.

Fig 1. Box-plots of variation in upper thermal tolerance (critical thermal maximum, CT_max) in component species of a tri-trophic system involving a caterpillar host (Manduca sexta), a wasp parasitoid (Cotesia congregata), and a wasp hyperparasitoid (Conura sp.).

Dashed lines = mean; solid lines = median; points = 5^th/95^th percentile outliers. Values inside boxes represent sample size (number of individuals). The means were different among all three species (One-way ANOVA with Tukey HSD post-hoc test; all P’s < 0.05). Photo credits: Justin Bredlau.

Fig 2. Variation in upper thermal tolerance (critical thermal maximum, CT_max) within the caterpillar host Manduca sexta in relation to ontogenetic stage (instar) and parasitism by the wasp Cotesia congregata.

Data points represent the mean ± 1 standard error. Values inside data points represent sample size (number of individuals). The main effects of instar and parasitism were both significant (Two-way ANOVA; Table 1).

Fig 3. Maximum daily air temperatures recorded near the study site in the past 124 years compared with the average critical thermal maximum (CT_max) of component H-P-HP species measured in this study.

Dashed lines: a = CT_max of host caterpillar, b = CT_max of parasitoid wasp, c = CT_max of hyperparasitoid wasp.