Developmental timing of extreme temperature events (heat waves) disrupts host–parasitoid interactions

Abstract

When thermal tolerances differ between interacting species, extreme temperature events (heat waves) will alter the ecological outcomes. The parasitoid wasp Cotesia congregata suffers high mortality when reared throughout development at temperatures that are nonstressful for its host, Manduca sexta. However, the effects of short‐term heat stress during parasitoid development are unknown in this host–parasitoid system. Here, we investigate how duration of exposure, daily maximum temperature, and the developmental timing of heat waves impact the performance of C. congregata and its host¸ M. sexta. We find that the developmental timing of short‐term heat waves strongly determines parasitoid and host outcomes. Heat waves during parasitoid embryonic development resulted in complete wasp mortality and the production of giant, long‐lived hosts. Heat waves during the 1st‐instar had little effect on wasp success, whereas heat waves during the parasitoid's nutritionally and hormonally critical 2nd instar greatly reduced wasp emergence and eclosion. The temperature and duration of heat waves experienced early in development determined what proportion of hosts had complete parasitoid mortality and abnormal phenotypes. Our results suggest that the timing of extreme temperature events will be crucial to determining the ecological impacts on this host–parasitoid system. Discrepancies in thermal tolerance between interacting species and across development will have important ramifications on ecosystem responses to climate change.

Upper thermal limits of Rhagoletis indifferens (Diptera: Tephritidae) pupae and pteromalid parasitoids (Hymenoptera: Pteromalidae) inside fly puparia

“…Perhaps there are differences in the cuticular compositions of pupae and immature wasps, when both are inside puparia, that allow the wasps to tolerate higher heat. In contrast to the host–parasite system here, thermal tolerances of host larval Manduca sexta (L.) (Lepidoptera: Sphingidae) are greater than of parasitic larval and adult Cotesia congregata (Say) (Hymenoptera: Braconidae) (Agosta et al 2018, Moore et al 2021), suggesting relative responses of insect hosts and their parasites to heat are specific to insect orders, species, and/or developmental stages.…”

“…indifferens puparia will also impact immature pteromalid wasps inside puparia, but whether the same treatments kill both flies and wasps is unknown. Upper thermal limits of larval host insects and adult or larval parasitoids can differ and thus might disrupt host–parasite interactions (e.g., Furlong and Zalucki 2017, Schreven et al 2017, Agosta et al 2018, Moore et al 2021, 2022). Identifying differences in heat tolerances between R .…”

Behavioral thermoregulation of caterpillars is altered by temperature, but not parasitism: An empirical field study

“…However, despite the occurrences of maximum temperatures above 40°C on multiple days (Appendix S2: Figure S6D), we did not observe the disruption of the host–parasitoid interaction seen at extreme high temperatures in laboratory conditions, where C. congregata suffer complete mortality and M. sexta hosts grow abnormally large and fail to undergo metamorphosis (Moore et al, 2021). Recent laboratory studies show that the temperature sensitivity of C. congregata during development is highly stage‐dependent (Moore et al, 2022). It is likely that, even with the experimental temperature manipulation, field conditions during our studies were not hot enough at the correct parasitoid stages to cause the disruption seen previously.…”

The interactive effects of heat stress, parasitism and host plant quality in a host–parasitoid system

“…To investigate the interactive effects of heat stress, parasitism and host plant identity, we implemented a fully factorial design, with sample sizes weighted towards the parasitized treatment groups to account for expected mortality. Based on prior studies (Malinski et al., 2023; Moore et al., 2020, 2021, 2022), we anticipated that our treatment groups would result in several system outcomes (Figure 1): (1) In the non‐parasitized, non‐heat‐shocked group, caterpillars would reach the pre‐pupal stage known as Wandering ; (2) In the non‐parasitized, heat‐shocked group, caterpillars would also reach the pre‐pupal stage of Wandering ; (3) In the parasitized non‐heat‐shocked group, caterpillar hosts would die upon successful Wasp Emergence ; and (4) In the parasitized heat‐shocked group, outcomes may include host death and Wasp Emergence , host death Without Wasp Emergence and host recovery of the pre‐pupal Wandering stage. We expected that these outcomes would be consistent across host plant types.…”

“…To investigate the interactive effects of heat stress, parasitism and host plant identity, we implemented a fully factorial design, with sample sizes weighted towards the parasitized treatment groups to account for expected mortality. Based on prior studies (Malinski et al, 2023;Moore et al, 2020Moore et al, , 2021Moore et al, , 2022, we anticipated that our treatment groups would result in several system outcomes (Figure 1):…”