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

Abstract

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 (CTmax) 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 wasp Cotesia congregata and its lepidopteran larval host, Manduca sexta. The growth of M. sexta was 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 by C. congregata wasps. 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 suggest C. congregata will suffer more severely under increasing temperatures than M. sexta, with cascading trophic and ecological effects. A free Plain Language Summary can be found within the Supporting Information of this article.

Effects of Simulated Heat Wave on Oxidative Physiology and Immunity in Asian Yellow Pond Turtle (Mauremys mutica)

“…However, many studies have exposed animals to different acute constant temperature heat waves, which unfortunately neglects the diurnal fluctuations in temperature under natural conditions (Dittmar et al, 2014;Leicht et al, 2019). This lack of ecological relevance may lead to misleading interpretations, as the performance of ectotherms is not always identical under constant and fluctuating thermal conditions (Bozinovic et al, 2011;Moore et al, 2021). Moreover, the biochemical and physiological responses to heat waves are still poorly understood in ectotherms, especially in non-avian reptiles, which are particularly vulnerable to climate warming (Bauerfeind and Fischer, 2014;Zhang et al, 2018).…”

Sperm Production Is Reduced after a Heatwave at the Pupal Stage in the Males of the Parasitoid Wasp Microplitisrufiventris Kok (Hymenoptera; Braconidae)

“…The mortality of adults is a measure that is currently recorded in studies of the consequences of stresses of insects. In most experimental works, the sex of insects is not provided, mainly because they are larvae [42], and in others, only females were tested [43]. Here again, comparative data on males are missing.…”

“…Interestingly, an experimental study on a pest moth showed that larvae, pupae, and adults are sensitive to a heatwave, resulting in a decrease in reproduction in both males and females [29]. This suggests that the larval stage of endoparasitoid may be also subject to physiological damages when their hosts were faced with unfavorable climatic conditions, as seen in Cotesia congregata during its larval stage inside its host Manduca sexta [42]. In koinobiont parasitoids, larvae could be less exposed to unfavorable temperatures because the host can move to find more suitable micro-environments, such as most mobile insects [44].…”

Connecting extreme climatic events to changes in ecological interactions

“…Phenotypic plasticity in heat tolerance has been demonstrated in many terrestrial and aquatic ectotherms (Seebacher et al., 2015), but the potential for plasticity to buffer the ecological impacts of EHTs is unclear (Gunderson & Stillman, 2015). Differences in heat tolerances between interacting species have been used to explore how EHTs can alter the outcomes of interspecific competition or host–parasite interactions (Comeault & Matute, 2021; Furlong & Zalucki, 2017; Moore et al., 2021; Schreven et al., 2017). Recent climate change may also play a role; recent evolutionary increases in heat tolerance or performance at high temperatures have been documented in several temperate insect systems (Diamond et al, 2017; Higgins et al, 2014).…”