Search for: All records

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. 

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.

 

ABSTRACT Climate change is increasing the frequency of heat waves and other extreme weather events experienced by organisms. How does the number and developmental timing of heat waves affect survival, growth and development of insects? Do heat waves early in development alter performance later in development? We addressed these questions using experimental heat waves with larvae of the tobacco hornworm, Manduca sexta. The experiments used diurnally fluctuating temperature treatments differing in the number (0–3) and developmental timing (early, middle and/or late in larval development) of heat waves, in which a single heat wave involved three consecutive days with a daily maximum temperature of 42°C. Survival to pupation declined with increasing number of heat waves. Multiple (but not single) heat waves significantly reduced development time and pupal mass; the best models for the data indicated that both the number and developmental timing of heat waves affected performance. In addition, heat waves earlier in development significantly reduced growth and development rates later in larval development. Our results illustrate how the frequency and developmental timing of sublethal heat waves can have important consequences for life history traits in insects. 

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.

 

1. Temperature strongly influences the rates of physiological processes in insects, including the herbivoreManduca sextaand its larval endoparasitoidCotesia congregata. Parasitisation byC. congregatadecreases the growth and consumption of food by larvalM. sexta. However, the effects of temperature on parasitised caterpillars and the developing wasp larvae are largely unknown.

2. In this study, parasitised and unparasitised caterpillars were reared at three constant temperatures (20, 25 and 30 °C) throughout larval development. Caterpillar mass gain and consumption were monitored daily until wandering (unparasitised control group) or wasp emergence (parasitised group) was observed. Development time and survival to emergence were measured as metrics of parasitoid performance.

3. ParasitisedM. sextadeveloped more slowly than unparasitised controls, but had similar cumulative consumption until the terminal instar. Parasitised caterpillars with relatively large parasitoid loads had higher rates of consumption and growth than those with smaller loads. Both temperature and parasitoid load strongly affected wasp success. Mean development time to wasp emergence increased with low temperatures and with large loads. The combination of warm temperature and large parasitoid loads greatly reduced wasp survival.

4. These results demonstrate the interactive effects of rearing temperature and parasitisation on host consumption and growth rates throughout larval development. In addition, wasp performance was affected by the interaction of temperature and parasitoid load size. High temperatures alter the dynamics of the interaction between the parasitoid and its caterpillar host, which could have far‐reaching impacts as the global temperatures continue to rise.