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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.

 

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 larvalPieris 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 ofP. rapaewithin North America vary in their sensitivity to nutritional balance and temperature.

 

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.

 

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. 

Evolutionary adaptation to temperature and climate depends on both the extent to which organisms experience spatial and temporal environmental variation (exposure) and how responsive they are to the environmental variation (sensitivity). Theoretical models and experiments suggesting substantial potential for thermal adaptation have largely omitted realistic environmental variation. Environmental variation can drive fluctuations in selection that slow adaptive evolution. We review how carefully filtering environmental conditions based on how organisms experience their environment and further considering organismal sensitivity can improve predictions of thermal adaptation. We contrast taxa differing in exposure and sensitivity. Plasticity can increase the rate of evolutionary adaptation in taxa exposed to pronounced environmental variation. However, forms of plasticity that severely limit exposure, such as behavioral thermoregulation and phenological shifts, can hinder thermal adaptation. Despite examples of rapid thermal adaptation, experimental studies often reveal evolutionary constraints. Further investigating these constraints and issues of timescale and thermal history are needed to predict evolutionary adaptation and, consequently, population persistence in changing and variable environments. 

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.

 

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, CT_max) and the mean or maximum environmental temperature it experiences. Yet, organisms face thermal stress and performance loss at body temperatures below their CT_max,and the steepness of that loss increases with the asymmetry of the thermal performance curve (TPC).

Global.

2015–2019.

Ants, fish, insects, lizards and phytoplankton.

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.

We find that the thermal optimum (T_opt, beyond which performance declines) is more labile than CT_max, inducing interspecific variation in asymmetry. Importantly, the degree of TPC asymmetry increases with T_opt. Thus, even though populations with higher T_opts in a hot environment might experience above‐optimal body temperatures less often than do populations with lower T_opts, they nonetheless experience steeper declines in performance at high body temperatures. Estimates of the annual cumulative decline in performance for temperatures above T_optsuggest that TPC asymmetry alters the onset, rate and severity of performance decrement at high body temperatures.

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.

 

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.