Geographic variation in the thermal sensitivity of life history traits has been widely documented in ectotherms, but the specific climatic factors that generate this variation are usually unknown. Invasive species that have recently expanded their geographic range provide useful systems for exploring plasticity and rapid evolution of life history and thermal biology along climatic gradients, but most studies consider a single life stage or a limited range of temperatures. We used North American populations of the invasive cabbage white butterfly (Pieris rapae) to explore these issues. We considered three geographic populations that differ in multiple aspects of seasonal climate, and measured thermal reaction norms of development rate, survival, and mass for both larval and pupal stages across a wide range of mean temperatures (16–34 °C). The optimal temperature ( 30 °C) for both larval and pupal development rates was similar for all three populations; and survival, development rates and pupal mass all declined at the highest mean temperature (34 °C). Low or high mean temperatures during larval development significantly reduced survival from pupation to adult eclosion. There were significant interactions between temperature and population for pupal and adult masses, reflecting the differing thermal reaction norms for size among these populations. However, these population differences do not suggest adaptation to local climatic conditions. We used these data to estimate thermal reaction norms for larval development rate, and developed a simple rate-summation model to predict development time to pupation in fluctuating thermal conditions. Lab experiments using ‘spring’ and ‘summer’ thermal conditions successfully predicted mean development time from hatching to pupation in both spring and summer conditions within 10

In insects and other invertebrates, prior pathogen exposures can improve immune responses and survival to subsequent infections through immune priming. Alternatively, stress and metabolic costs of multiple infections can impair host immunity and survival. The effects of high-temperature extremes on host-pathogen interactions are not well understood despite the increasing occurrence of heat waves caused by climate change. The response of insects to heat waves and pathogens depends on recent evolutionary history with selective pressures. Domestication of insect pests has occurred in lab colonies of model species, reducing selective pressures for immune and heat stress responses. Lab strains are often used in immunological or heat stress experiments to represent wild field strains, but the efficacy of this approach is seldom evaluated. Using the tobacco hornworm (Manduca sexta), we tested the impact of a heat wave during initial pathogen exposure on survival of a secondary infection with Bacillus thuringiensis bacteria. We used a domesticated lab population and a naturally occurring field population of M. sexta to evaluate the impacts of recent domestication on immune and thermal responses. A heat wave during initial infection significantly increased survival of the secondary B. thuringiensis infection in the field, but not the lab population of M. sexta. In the field population, survival of the repeated infection was temperature dependent: exposure to an initial infection event reduced survival of the secondary infection at the control temperature regime, consistent with a stress effect. However, a heat wave during the initial infection event increased survival of the secondary infection, consistent with immune priming effects. The results of this study demonstrate that (a) insect response to thermal stress and pathogens can depend on recent domestication and (b) responses of hosts to repeat pathogen exposures can be temperature-dependent, suggesting that cross-talk between the heat stress and immune memory pathways may have important consequences for host-pathogen outcomes under heat wave events.Read the free Plain Language Summary for this article on the Journal blog.

Climate change has been repeatedly linked to phenological shifts in many taxa, but the factors that drive variation in phenological sensitivity remain unclear. For example, relatively little is known about phenological responses in areas that have not exhibited a consistent warming trend, making it difficult to project phenological responses in response to future climate scenarios for these regions. We used an extensive community science dataset to examine changes in the adult flight onset dates of 38 butterfly species with interannual variation in spring temperatures in the Piedmont region of North Carolina, a region that did not experience a significant overall warming trend in the second half of the 20th century. We also explored whether voltinism, overwintering stage, and mean adult flight onset dates explain interspecific variation in phenological sensitivity to spring temperature. We found that 12 out of 38 species exhibited a significant advance in adult flight onset dates with higher spring temperatures. In comparison, none of the 38 species exhibited a significant advance with year. There was a significant interaction between mean onset flight date and voltinism, such that late-emerging, multivoltine species tended to be the most sensitive to spring temperature changes. We did not observe a significant correlation between phenological sensitivity and the overwintering stage. These results suggest that butterfly arrival dates may shift as temperatures are projected to rise in the southeastern United States, with late-emerging, multivoltine species potentially exhibiting the greatest shifts in adult flight onset dates.

The effects of temperature on reproduction and other key fitness traits are often primarily considered only for the adult thermal environment, but exposure to thermal stress during earlier life stages may carry over to influence adult traits within a generation or even across generations. In this study, we assessed how an acute heat shock event experienced at two different points in Manduca sexta larval development (early and late) impacted adult performance and fitness traits and whether thermal exposure of parents elicited plastic changes in offspring traits. Heat stress during late larval development had significantly greater negative impacts on adult performance and fitness compared to earlier exposure. Adults that experienced a late larval heat shock failed to produce any viable offspring due to complete elimination of egg hatching success. Larval heat stress during the parental generation also reduced larval development times of their offspring in both control and heat shock conditions. The results of this study illustrate the negative consequences of larval heat stress for adult fitness and indicate that the parental early thermal environment can significantly influence some traits in the next generation. The effects of parent environmental conditions during development, and not just at the adult stage, may therefore be an important but often overlooked factor when assessing cumulative fitness impacts across generations and predicting the vulnerability of populations to climate change.

Thermal performance curves (TPCs) depict variation in vital rates in response to temperature and have been an important tool to understand ecological and evolutionary constraints on the thermal sensitivity of ectotherms. TPCs allow for the calculation of indicators of thermal tolerance, such as minimum, optimum, and maximum temperatures that allow for a given metabolic function. However, these indicators are computed using only responses from surviving individuals, which can lead to underestimation of deleterious effects of thermal stress, particularly at high temperatures. Here, we advocate for an integrative framework for assessing thermal sensitivity, which combines both vital rates and survival probabilities, and focuses on the temperature interval that allows for population persistence. Using a collated data set of Lepidopteran development rate and survival measured on the same individuals, we show that development rate is generally limiting at low temperatures, while survival is limiting at high temperatures. We also uncover differences between life stages and across latitudes, with extended survival at lower temperatures in temperate regions. Our combined performance metric demonstrates similar thermal breadth in temperate and tropical individuals, an effect that only emerges from integration of both development and survival trends. We discuss the benefits of using this framework in future predictive and management contexts.

Ongoing climate change is increasing the frequency and magnitude of high-temperature events (HTEs), causing heat stress in parasitoids and their hosts. We argue that HTEs and heat stress should be viewed in terms of the intersecting life cycles of host and parasitoid. Recent studies illustrate how the biological consequences of a given HTE may vary dramatically depending on its timing within these lifecycles. The temperature sensitivity of host manipulation by parasitoids, and by viral endosymbionts of many parasitoids, can contribute to differing responses of hosts and parasitoids to HTEs. In some cases, these effects can result in reduced parasitoid success and increased host herbivory and may disrupt the ecological interactions between hosts and parasitoids. Because most studies to date involve endoparasitoids of aphid or lepidopteran hosts in agricultural systems, our understanding of heat responses of host-parasitoid interactions in natural systems is quite limited.

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 free Plain Language Summary for this article on the Journal blog. Read the free Plain Language Summary for this article on the Journal blog.image

Climate warming is considered to be among the most serious of anthropogenic stresses to the environment, because it not only has direct effects on biodiversity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly in terms of threats to species preservation, as well as in the preservation of an array of ecosystem services provided by biodiversity. Among the most affected groups of animals are insects-central components of many ecosystems-for which climate change has pervasive effects from individuals to communities. In this contribution to the scientists' warning series, we summarize the effect of the gradual global surface temperature increase on insects, in terms of physiology, behavior, phenology, distribution, and species interactions, as well as the effect of increased frequency and duration of extreme events such as hot and cold spells, fires, droughts, and floods on these parameters. We warn that, if no action is taken to better understand and reduce the action of climate change on insects, we will drastically reduce our ability to build a sustainable future based on healthy, functional ecosystems. We discuss perspectives on relevant ways to conserve insects in the face of climate change, and we offer several key recommendations on management approaches that can be adopted, on policies that should be pursued, and on the involvement of the general public in the protection effort.

Feeding for most animals involves bouts of active ingestion alternating with bouts of no ingestion. In insects, the temporal patterning of bouts varies widely with resource quality and is known to affect growth, development time, and fitness. However, the precise impacts of resource quality and feeding behavior on insect life history traits are poorly understood. To explore and better understand the connections between feeding behavior, resource quality, and insect life history traits, we combined laboratory experiments with a recently proposed mechanistic model of insect growth and development for a larval herbivore, Manduca sexta. We ran feeding trials for 4th and 5th instar larvae across different diet types (two hostplants and artificial diet) and used these data to parameterize a joint model of age and mass at maturity that incorporates both insect feeding behavior and hormonal activity. We found that the estimated durations of both feeding and nonfeeding bouts were significantly shorter on low-quality than on high-quality diets. We then explored how well the fitted model predicted historical out-of-sample data on age and mass of M. sexta. We found that the model accurately described qualitative outcomes for the out-of-sample data, notably that a low-quality diet results in reduced mass and later age at maturity compared with high-quality diets. Our results clearly demonstrate the importance of diet quality on multiple components of insect feeding behavior (feeding and nonfeeding) and partially validate a joint model of insect life history. We discuss the implications of these findings with respect to insect herbivory and discuss ways in which our model could be improved or extended to other systems.

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.

Temperature affects rates of ingestion, growth and other key processes in insects and other ectotherms, a relationship described by the thermal performance curve. But the history of temperature exposure can cause stress or acclimation responses, altering the relationship between current temperature and performance. The temporal dynamics of such time-dependent effects for ectotherm growth are poorly understood. We quantify how growth and ingestion change over time at different constant temperatures during the final larval instar for two thermal-generalist insect species, Pieris rapae L. and Manduca sexta L . Initial growth rates were greatest at higher temperatures for both P. rapae (29-35 °C) and M. sexta (34-38 °C); but growth rates at higher temperatures declined over time. As a result, the optimal and maximal temperatures for growth declined over time (2-4 days) in both species. Unlike P. rapae , M. sexta could maintain growth and survival to wandering and pupation at temperatures above 35 °C. For M. sexta larvae at 40 °C, ingestion continues even as growth declines, suggesting that post-ingestive processes limit growth rates at these high temperatures. Our results show how time-dependent effects at higher temperatures develop over hourly to daily time scales, with important consequences for understanding and modeling organismal responses to heat waves and extreme temperature events.

The interaction between larval host plant quality and temperature can influence the short-term physiological rates and life-history traits of insect herbivores. These factors can vary locally, resulting in local adaptation in responses to diet and temperature, but the comparison of these interactions between populations is infrequently carried out. In this study, we examine how the macronutrient ratio of an artificial diet determines the larval growth, development, and survival of larval Pieris rapae (Lepidoptera: Pieridae) at different temperatures between two invasive North American populations from different climatic regions. We conducted a fully factorial experiment with three temperature treatments (18°C, 25°C, and 32°C) and three artificial diet treatments varying in terms of the ratio of protein to carbohydrate (low protein, balanced, and high protein). The effects of diet on life-history traits were greater at lower temperatures, but these differed between populations. Larvae from the subtropical population had reduced survival to pupation on the low-protein diet in the cold temperature treatment, whereas larval survival for the temperate population was equally high for all temperature and diet treatments. Overall, both populations performed more poorly (i.e., they showed slower rates of consumption, growth, and development, and had a smaller pupal mass) in the diet with the low protein ratio, but larvae from the temperate population were less sensitive to diet ratio changes at all temperatures. Our results confirm that the physiological and life-history consequences of imbalanced nutrition for insect herbivores may depend on developmental temperatures, and that different geographic populations of P. rapae within North America vary in their sensitivity to nutritional balance and temperature.

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.

Aim Understanding and predicting the biological consequences of climate change requires considering the thermal sensitivity of organisms relative to environmental temperatures. One common approach involves 'thermal safety margins' (TSMs), which are generally estimated as the temperature differential between the highest temperature an organism can tolerate (critical thermal maximum, CTmax) and the mean or maximum environmental temperature it experiences. Yet, organisms face thermal stress and performance loss at body temperatures below their CTmax, and the steepness of that loss increases with the asymmetry of the thermal performance curve (TPC). Location Global. Time period 2015-2019. Major taxa studied Ants, fish, insects, lizards and phytoplankton. Methods We examine variability in TPC asymmetry and the implications for thermal stress for 384 populations from 289 species across taxa and for metrics including ant and lizard locomotion, fish growth, and insect and phytoplankton fitness. Results We find that the thermal optimum (T-opt, beyond which performance declines) is more labile than CTmax, inducing interspecific variation in asymmetry. Importantly, the degree of TPC asymmetry increases with T-opt. Thus, even though populations with higher T(opt)s in a hot environment might experience above-optimal body temperatures less often than do populations with lower T(opt)s, they nonetheless experience steeper declines in performance at high body temperatures. Estimates of the annual cumulative decline in performance for temperatures above T-opt suggest that TPC asymmetry alters the onset, rate and severity of performance decrement at high body temperatures. Main conclusions Species with the same TSMs can experience different thermal risk due to differences in TPC asymmetry. Metrics that incorporate additional aspects of TPC shape better capture the thermal risk of climate change than do TSMs.

In nature, plant-insect interactions occur in complex settings involving multiple trophic levels, often with multiple species at each level.(1) Herbivore attack of a host plant typically dramatically alters the plant's odor emission in terms of concentration and composition.(2,3) Therefore, a well-adapted herbivore should be able to predict whether a plant is still suitable as a host by judging these changes in the emitted bouquet Although studies have demonstrated that oviposition preferences of successive insects were affected by previous infestations,(4,5) the underlying molecular and olfactory mechanisms remain unknown. Here, we report that tobacco hawkmoths (Manduca sexta) preferentially oviposit on Jimson weed (Datura wrightii) that is already infested by a specialist, the three-lined potato beetle (Lema daturaphila). Interestingly, the moths' offspring do not benefit directly, as larvae develop more slowly when feeding together with Lema beetles. However, one of M. sexta's main enemies, the parasitoid wasp Cotesia congregata, prefers the headspace of M. sexta-infested plants to that of plants infested by both herbivores. Hence, we conclude that female M. sexta ignore the interspecific competition with beetles and oviposit deliberately on beetle-infested plants to provide their offspring with an enemy-reduced space, thus providing a trade-off that generates a net benefit to the survival and fitness of the subsequent generation. We identify that alpha-co-paene, emitted by beetle-infested Datura, plays a role in this preference. By performing heterologous expression and single-sensillum recordings, we show that odorant receptor (Or35) is involved in fx-copaene detection.

In tree canopies, incoming solar radiation interacts with leaves and branches to generate temperature differences within and among leaves, presenting thermal opportunities and risks for leaf-dwelling ectotherms. Although leaf biophysics and insect thermal ecology are well understood, few studies have examined them together in single systems. We examined temperature variability in aspen canopies, Populus tremuloides, and its consequences for a common herbivore, the leaf-mining caterpillar Phyllocnistis populiella. We shaded leaves in the field and measured effects on leaf temperature and larval growth and survival. We also estimated larval thermal performance curves for feeding and growth and measured upper lethal temperatures. Sunlit leaves directly facing the incoming rays reached the highest temperatures, typically 3-8 degrees C above ambient air temperature. Irradiance-driven increases in temperature, however, were transient enough that they did not alter observed growth rates of leaf miners. Incubator and ramping experiments suggested that larval performance peaks between 25 and 32 degrees C and declines to zero between 35 and 40 degrees C, depending on the duration of temperature exposure. Upper lethal temperatures during 1-h heat shocks were 42-43 degrees C. When larvae were active in early spring, temperatures generally were low enough to depress rates of feeding and growth below their maxima, and only rarely did estimated mine temperatures rise beyond optimal temperatures. Observed leaf or mine temperatures never approached larval upper lethal temperatures. At this site during our experiments, larvae thus appeared to have a significant thermal safety margin; the more pressing problem was inadequate heat. Detailed information on mine temperatures and larval performance curves, however, allowed us to leverage long-term data sets on air temperature to estimate potential future shifts in performance and longer-term risks to larvae from lethally high temperatures. This analysis suggests that, in the past 20 years, larval performance has often been limited by cold and that the risk of heat stress has been low. Future warming will raise mean rates of feeding and growth but also the risk of exposure to injuriously or lethally high temperatures.

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.