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1. Differing thermal sensitivities in a host–parasitoid interaction: High, fluctuating developmental temperatures produce dead wasps and giant caterpillars

   https://doi.org/10.1111/1365-2435.13748  

   Moore, M. Elizabeth ; Hill, Christina A. ; Kingsolver, Joel G. ; Marshall, ed., Katie ( March 2021 , Functional Ecology)

   Insect parasitoids, and the arthropod hosts they consume during development, are important ecological players in almost all environments across the globe. As ectothermic organisms, both parasitoid and host are strongly impacted by environmental temperature. If thermal tolerances differ between host insect and parasitoid, then the outcome of their interaction will be determined by the ambient temperature. As mean temperatures continue to rise and extreme temperatures become more frequent, we must determine the effect of high temperature stress on host–parasitoid systems to predict how they will fare in the face of climate change.

   The majority of studies conducted on host–parasitoid systems focus on either performance under constant temperature or a fixed metric of thermal tolerance (CT_max) for individual organisms. However, performance at constant temperatures is not predictive of performance under ecologically relevant, fluctuating temperatures and measurements of thermal thresholds provide little information regarding the effects of temperature throughout development. We address this by testing the effects of increasing mean temperature in both constant and fluctuating (±10°C) environments throughout development on the performance of the parasitoid waspCotesia congregataand its lepidopteran larval host,Manduca sexta.

   The growth ofM. sextawas influenced by mean temperature, diurnal fluctuations and parasitization status. Caterpillar growth rate increased with increasing mean temperature, but decreased in response to diurnal fluctuations and parasitization byC. congregatawasps.

   Wasp survival decreased with increasing mean temperature and with diurnal fluctuations. The effect of diurnal fluctuations was stronger at higher mean temperatures. Diurnal fluctuations at our highest mean temperature treatment (30 ± 10°C) resulted in complete wasp mortality, and parasitized hosts displayed abnormal physiology, wherein they failed to exhibit wasp emergence, did not enter the prepupal stage, continued to feed and grew up to twofold larger than a normal, unparasitized caterpillar.

   Our results indicate hosts and parasitoids in this system have different thermal tolerances during development; the parasitoid wasp suffered complete mortality at a temperature regime that is mildly stressful for the unparasitized caterpillar host species. Our findings suggestC. congregatawill suffer more severely under increasing temperatures thanM. sexta, with cascading trophic and ecological effects.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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

   https://doi.org/10.1002/ece3.8618  

   Moore, Megan Elizabeth ; Hill, Christina A. ; Kingsolver, Joel G. ( March 2022 , Ecology and Evolution)

   When thermal tolerances differ between interacting species, extreme temperature events (heat waves) will alter the ecological outcomes. The parasitoid waspCotesia congregatasuffers 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 ofC.congregataand 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.

    

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

   https://doi.org/10.1002/ecs2.4578  

   Moore, M. Elizabeth ; Alston, Meggan A. ; Kingsolver, Joel G. ( June 2023 , Ecosphere)

   Laboratory assays show that parasites often have lower heat tolerance than their hosts. But how physiological tolerances and behavioral responses of hosts and parasites combine to affect their ecological interactions in heterogeneous field environments is largely unknown. We addressed this challenge using the model insect system of the braconid wasp parasitoid,Cotesia congregata, and its caterpillar host,Manduca sexta. We used experimental manipulations of microclimate in the field to determine how elevated daytime temperatures altered the behavior, performance, and survival of host and parasite. Our experimental manipulation increased daily maximum temperatures on host plants, but had negligible effects on overall mean temperature. These increased maximum temperatures resulted in subtle, biologically relevant, changes in physiology and behavior of the host and parasitoid. We found that parasitism by the wasp did not significantly alter caterpillar thermoregulatory behavior, while experimentally increased daily maximum temperatures resulted in both parasitized and unparasitized caterpillars to be found more frequently in cooler microhabitats. Overall, we did not observe the complete parasitoid mortality seen at extreme temperatures in laboratory studies, but gained insight into the sublethal effects of increased daily maximum temperatures on host and parasitoid behavior and physiology. Climate change will alter both the biotic and abiotic environments that organisms face, and we show here that empirical experiments in the field are important for understanding organismal response to these new environments.

    

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4. Host species differences in the thermal mismatch of host–parasitoid interactions

   https://doi.org/10.1242/jeb.245702  

   Malinski, Katherine H. ; Sorenson, Clyde E. ; Moore, M. Elizabeth ; Willett, Christopher S. ; Kingsolver, Joel G. ( June 2023 , Journal of Experimental Biology)

   ABSTRACT Extreme high temperatures associated with climate change can affect species directly, and indirectly through temperature-mediated species interactions. In most host–parasitoid systems, parasitization inevitably kills the host, but differences in heat tolerance between host and parasitoid, and between different hosts, may alter their interactions. Here, we explored the effects of extreme high temperatures on the ecological outcomes – including, in some rare cases, escape from the developmental disruption of parasitism – of the parasitoid wasp, Cotesia congregata, and two co-occurring congeneric larval hosts, Manduca sexta and M. quinquemaculata. Both host species had higher thermal tolerance than C. congregata, resulting in a thermal mismatch characterized by parasitoid (but not host) mortality under extreme high temperatures. Despite parasitoid death at high temperatures, hosts typically remain developmentally disrupted from parasitism. However, high temperatures resulted in a partial developmental recovery from parasitism (reaching the wandering stage at the end of host larval development) in some host individuals, with a significantly higher frequency of this partial developmental recovery in M. quinquemaculata than in M. sexta. Hosts species also differed in their growth and development in the absence of parasitoids, with M. quinquemaculata developing faster and larger at high temperatures relative to M. sexta. Our results demonstrate that co-occurring congeneric species, despite shared environments and phylogenetic histories, can vary in their responses to temperature, parasitism and their interaction, resulting in altered ecological outcomes. 

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

   https://doi.org/10.1111/1365-2435.14498  

   Parker, Anna L. ; Kingsolver, Joel G. ( January 2024 , Functional Ecology)

   Species interactions are expected to change in myriad ways as the frequency and magnitude of extreme temperature events increase with anthropogenic climate change.

   The relationships between endosymbionts, parasites and their hosts are particularly sensitive to thermal stress, which can have cascading effects on other trophic levels.

   We investigate the interactive effects of heat stress and parasitism on a terrestrial tritrophic system consisting of two host plants (one common, high‐quality plant and one novel, low‐quality plant), a caterpillar herbivore and a specialist parasitoid wasp.

   We used a fully factorial experiment to determine the bottom‐up effects of the novel host plant on both the caterpillars' life history traits and the wasps' survival, and the top‐down effects of parasitism and heat shock on caterpillar developmental outcomes and herbivory levels.

   Host plant identity interacted with thermal stress to affect wasp success, with wasps performing better on the low‐quality host plant under constant temperatures but worse under heat‐shock conditions.

   Surprisingly, caterpillars consumed less leaf material from the low‐quality host plant to reach the same final mass across developmental outcomes.

   In parasitized caterpillars, heat shock reduced parasitoid survival and increased both caterpillar final mass and development time on both host plants.

   These findings highlight the importance of studying community‐level responses to climate change from a holistic and integrative perspective and provide insight into potential substantial interactions between thermal stress and diet quality in plant–insect systems.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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