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  1. Abstract

    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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  2. 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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    Free, publicly-accessible full text available June 15, 2024
  3. Abstract

    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. 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. 
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  5. Abstract

    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 ofM. 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.

     
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  6. Abstract 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 (Topt, beyond which performance declines) is more labile than CTmax, inducing interspecific variation in asymmetry. Importantly, the degree of TPC asymmetry increases with Topt. Thus, even though populations with higher Topts in a hot environment might experience above‐optimal body temperatures less often than do populations with lower Topts, they nonetheless experience steeper declines in performance at high body temperatures. Estimates of the annual cumulative decline in performance for temperatures above Toptsuggest 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.

     
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  7. null (Ed.)
    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. 
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  8. Abstract

    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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