Chun-Sen Ma
email: machunsen@caas.cn

Gang Ma
email: magang@caas.cn

Sylvain Pincebourde
email: sylvainpincebourde@univ-tours.fr

Survive a Warming Climate: Insect Responses to Extreme High Temperatures

Keywords: climate change, extreme climate, life history trait, demographics, heat tolerance, thermoregulation

Global change includes a substantial increase in the frequency and intensity of extreme high temperatures (EHTs) which influence insects at almost all levels. The number of studies showing the ecological importance of EHTs has risen in recent years but the knowledge is rather dispersed in the contemporary literature. Here we reviewed the biological and ecological effects of EHTs actually experienced in the field, i.e. when coupled to fluctuating thermal regimes. First, we characterized EHTs in the field. Then, we summarized the impacts of EHTs on insects at various levels and the processes allowing insects to buffer EHTs. Finally, we argue that the mechanisms leading to positive or negative impacts of EHTs on insects can only be resolved from integrative approaches considering natural thermal regimes. Thermal extremes, perhaps more than the gradual increase in mean temperature, drive insect responses to climate change, with crucial impact on pest management and biodiversity conservation.

INTRODUCTION

Temperature varies across temporal and spatial scales in terrestrial and aquatic ecosystems [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]117). Most insect species experience thermal fluctuations that can involve sublethal or lethal extreme high temperatures (EHTs) which affect physiological processes [START_REF] Feder | Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae[END_REF] and ecological systems [START_REF] Easterling | Climate extremes: observations, modeling, and impacts[END_REF]. Frequent EHTs may even lead to adaptive evolution in insects [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]. For decades, however, most studies concerning thermal effects on insects concentrated on the response to mean temperature or to fluctuations within the tolerable range while ignoring variations in the characteristics of EHTs (89, 105). Recently, researchers realized the biological and ecological importance of fluctuating temperature regimes but little attention is paid to the impacts of ecologically-relevant EHTs [START_REF] Buckley | Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities[END_REF].

Global climate change includes a substantial increase in the occurrence of EHTs [START_REF] Alexander | Global observed changes in daily climate extremes of temperature and precipitation[END_REF][START_REF]Summary for policymakers[END_REF], and this increase will continue in the near future (96). By contrast, the occurrence of cold extremes (cold spells, cold nights) is largely decreasing [START_REF] Alexander | Global observed changes in daily climate extremes of temperature and precipitation[END_REF][START_REF] Easterling | Climate extremes: observations, modeling, and impacts[END_REF].

Thus, in a warming world, insects will be challenged mostly by elevated body temperatures [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]. Neglecting daily temperature extremes generates inaccurate predictions when modeling the impacts of climate warming on populations (89). The key role of EHTs in the response of insects to warming is now attracting more attention and there is an urgent need to synthesize the disparate works. Here, we provide an overview of how natural EHTs impact insect performance at individual, population and community levels, by considering that EHTs are filtered by microhabitats and buffered by insects through behavioral thermoregulation, phenotypic plasticity (e.g., acclimation), ontogeny variation, adaptive evolution and the resilience of their network (Figure 1). Our synthesis complements previous works that focused on the effects of low temperatures (125), or increase in mean temperature (119) and fluctuation regimes [START_REF] Colinet | Insects in fluctuating thermal environments[END_REF], to finally provide a comprehensive understanding of the impact of climate change on insects.

HOW DO WE CHARACTERIZE THERMAL EXTREMES?

Definition and description of extreme high temperatures

Until recently, no unified definition of EHTs existed in an environmental perspective.

Meteorologists define EHTs as the temperatures above the 90th, 95th or 99th percentile of temperature distributions [START_REF] Alexander | Global observed changes in daily climate extremes of temperature and precipitation[END_REF][START_REF]Summary for policymakers[END_REF], and similar indices are used by ecologists [START_REF] Buckley | Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities[END_REF]. The definition of EHTs can also be based on their societal impacts.

The historical heat wave that hit Europe in 2003 is often used as a reference [START_REF] Battisti | A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly[END_REF].

Finally, another definition comes from biology, with environmental temperature exceeding upper physiological thresholds of focal organisms (96). Overall, a hybrid definition for EHTs corresponds to an "episode where climate or climate-driven conditions trigger a negative threshold-like (non-linear) biological response" [START_REF] Bailey | Tackling extremes: challenges for ecological and evolutionary research on extreme climatic events[END_REF].

The variables used to characterize EHTs are highly variable among studies, resulting in difficulties to compare directly their results. Most studies on EHTs are opportunistic and usually lacking replication (126). Controlled field experiments often simulate a single level of a given climate extreme imposed at a small spatial scale (126). The lack of a clear description of characteristics of EHTs limits our understanding of how such irregular EHTs affect biological systems [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF]87,92,122). Thus, resolving the main components of EHTs becomes more meaningful than a general definition for ecological research (Figure 2). Based on field temperature data including EHTs (87), we identified several important characteristics: daily maximum and minimum temperatures which define the daily amplitude during the EHT events; the frequency of EHT events over long temporal scale (typically the number of hot days during a given period); the time elapsed between each subsequent EHT event, defining the temporal variance of extreme events. By manipulating values of each variable and their combinations, experimental designs in laboratory, mesocosms or in the field can quantify the impacts of EHTs with varying intensity, frequency, duration and temporal variance on fitness-related life history traits and demography (Figure 2).

In the field, insects experience temperature cycles with a single or several successive hot days alternating with a few mild days (87, 148). Diurnal cycles also alternate several hot hours around mid-day with mild hours (89, 147). Thus, the effects of EHTs depend largely on theirs characteristics which are complex to describe and to simulate in the lab or mesocosms due to the stochastic nature of EHTs.

Intensity, duration and frequency are often used to link ecological performance and EHTs [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF]92,122), despite the high uncertainty in these metrics. Simple statistical characteristics of EHTs were designed to explore the impact of different temperatures during daytime (89) and nighttime (147), different frequencies of hot days (86,145) and different amplitude of fluctuation (140). During hot events, insects can be injured by EHTs approaching their physiological thresholds but the mild temperatures between hot events allow insects to repair [START_REF] Bai | Independent and combined effects of daytime heat stress and nighttime recovery determine thermal performance[END_REF]87). The temporal sequence of hot and mild phases is therefore an important characteristic of EHTs (87, 148). The impact of EHTs should be a subtle balance between heat injury and recovery [START_REF] Bai | Independent and combined effects of daytime heat stress and nighttime recovery determine thermal performance[END_REF]87,148).

Thermal extreme vs. mean temperature

Thermal performance curves (TPCs) are often used to describe the response of biological performance to temperature based on constant temperature treatments (124).

TPCs are asymmetrical and nonlinear, thereby generating Jensen's inequality (120) which is used to describe the biological effects of environmental variability [START_REF] Denny | The fallacy of the average: on the ubiquity, utility and continuing novelty of Jensen's inequality[END_REF].

TPCs, combined with Jensen's inequality, are frequently used to compute insect performance under fluctuating/changing temperatures, feeding predictions of climate change impacts [START_REF] Bozinovic | The mean and variance of environmental temperature interact to determine physiological tolerance and fitness[END_REF][START_REF] Kingsolver | Heat stress and the fitness consequences of climate change for terrestrial ectotherms[END_REF]105,124,134). Based on Jensen's inequality, the effects of temperature variation would be positive, small and dramatically negative at low, intermediate and high temperatures, respectively [START_REF] Denny | The fallacy of the average: on the ubiquity, utility and continuing novelty of Jensen's inequality[END_REF][START_REF] Koussoroplis | Understanding and predicting physiological performance of organisms in fluctuating and multifactorial environments[END_REF]. The left-skewed TPCs show that the thermal optimum (Topt) is close to the critical thermal maximum (CTmax), meaning that even a small variation in mean temperature above Topt can push insects over CTmax, leading to dramatic decline in performance and fitness (105).

By causing an increase in thermal variance and in the strength of the Jensen's inequality, EHTs negatively impact insect fitness even if mean temperature remains near the optimal range (87, 89, 105). Indeed, the impact of increasing variance on key traits related to fitness can be larger than an increase in mean temperature (89, 105, 140). Greater variance caused by EHTs can lead to decreased maximum performance, truncated thermal performance breadth and narrow thermal safety margin (105, 134). However, ambient temperature fluctuates usually with reasonable amplitude up to sublethal daily maxima. Near-optimal temperature may occur during some parts of the day (e.g., morning, night) and thus provide an opportunity for insects to recover from heat injuries occurring around midday (87, 148). A better performance is therefore expected under variable regimes than under constant high temperatures. For example, temperature variation can improve rather than depress the development of aphids when the mean temperature is higher than the Topt for development, thereby challenging the "Kaufmann effect" (147). Importantly, using TPCs derived from constant temperatures to predict insect fitness in field conditions contains the unrealistic assumption that performance is independent of thermal history, rates of temperature change and exposure times (124). More work on the thermal responses to the EHT characteristics will certainly help to design novel approaches to draw TPCs that could incorporate the influence of EHTs on insect performance and fitness.

The seasonal and diurnal patterns of EHTs

The amplitude of warming, including more frequent and intense extremes, is higher in spring, autumn and winter than in summer [START_REF] Alexander | Global observed changes in daily climate extremes of temperature and precipitation[END_REF][START_REF]Summary for policymakers[END_REF]. However, the biological impacts of EHTs in these seasons are relatively overlooked. EHTs in spring affect the phenological synchronization between plants and herbivore insects [START_REF] Kudo | Early onset of spring increases the phenological mismatch between plants and pollinators[END_REF]115) and parasitoids [START_REF] Evans | Warm springs reduce parasitism of the cereal leaf beetle through phenological mismatch[END_REF]. EHTs in autumn may affect diapause induction, subsequent overwintering survival and spring population growth (132). EHTs in winter may influence survival during diapause and post-diapause development [START_REF] Bokhorst | Extreme winter warming events more negatively impact small rather than large soil fauna: shift in community composition explained by traits not taxa[END_REF]127).

Individuals of univoltine species can experience EHTs across different seasons (118).

Yet we have little information on seasonal stage-specific responses and their consequences at the population level. Moreover, the amplitude of nighttime warming is higher than daytime warming [START_REF] Alexander | Global observed changes in daily climate extremes of temperature and precipitation[END_REF][START_REF]Summary for policymakers[END_REF]. Nighttime warming leads to contrasting effects on thermal performance and fitness, in contradiction with the predictions based on constant temperatures (147) or daytime warming [START_REF] Barton | Opposite effects of daytime and nighttime warming on top-down control of plant diversity[END_REF]89). To date, however, only few studies explored the specific effects of diurnal vs. nocturnal patterns of EHTs on insects [START_REF] Bai | Independent and combined effects of daytime heat stress and nighttime recovery determine thermal performance[END_REF][START_REF] Barton | Opposite effects of daytime and nighttime warming on top-down control of plant diversity[END_REF]89,147).

HOW DO INSECTS RESPOND TO THERMAL EXTREMES?

3.1. Physiological, biochemical and symbiont responses

Mechanisms underlying heat damage

Heat damage in insects involves a series of disorders at the molecular, biochemical and physiological levels [START_REF] Bowler | Heat death in poikilotherms: Is there a common cause?[END_REF][START_REF] Chown | Insect Physiological Ecology: Mechanisms and Patterns[END_REF]. Heat-induced changes in the fluidity of phospholipidic membranes and cellular homeostasis initiate heat damage [START_REF] Bowler | Heat death in poikilotherms: Is there a common cause?[END_REF]. The OCLTT hypothesis (oxygen and capacity limitation of thermal tolerance) proposes that performance is constrained by the capacity for oxygen delivery relative to oxygen demand. The delivery of oxygen is the limiting factor during EHTs [START_REF] Ern | A mechanistic oxygen-and temperature-limited metabolic niche framework[END_REF]114). This hypothesis was confirmed in several aquatic species (135). However, it is not generally applicable to terrestrial insects since they are unlikely to become oxygen limited [START_REF] Bowler | Heat death in poikilotherms: Is there a common cause?[END_REF][START_REF] Lehmann | Oxygen limitation is not the cause of death during lethal heat exposure in an insect[END_REF], except if they live in close microenvironment such as plant galls (109). Finally, EHTs can disrupt the cellular ion balance (hyperkalemia), thereby impairing neurophysiological functions (103) and damaging mitochondria [START_REF] Bowler | Heat death in poikilotherms: Is there a common cause?[END_REF].

Physiological and molecular responses

Insects can produce and accumulate particular molecules to prevent protein denaturation or cell inactivation during EHTs. Polyols, e.g. mannitol in Aphis gossypii and sorbitol in Bemisia argentifolii, are accumulated to cope with daytime EHTs [START_REF] Hendrix | Polyol metabolism in homopterans at high temperatures: accumulation of mannitol in aphids (Aphididae: Homoptera) and sorbitol in whiteflies (Aleyrodidae: Homoptera)[END_REF].

Mannitol and sorbitol quantities were higher at noon than during early morning.

Heat-shock proteins (Hsps) [START_REF] Feder | Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae[END_REF][START_REF] Lopez-Martinez | Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress[END_REF] and cuticle proteins (102) are induced and/or accumulated to deal with EHTs. Apple maggots express Hsp increasingly from midday to peak in late afternoon, paralleling the dynamics of air and fruit temperature in summer [START_REF] Lopez-Martinez | Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress[END_REF]. Locusts are more heat-tolerant at low-than at high-latitude as a result of their expression pattern of Hsp70 and Hsp90 [START_REF] Chen | Evolution of heat-shock protein expression underlying adaptive responses to environmental stress[END_REF]. The potato aphid increases concentration of several exoskeletal proteins during heat stress (102).

Symbiont-mediated responses

Bacterial endosymbionts provide essential nutrients to their insect host. EHTs depress the diversity, abundance and activity of endosymbionts, decreasing heat tolerance and fitness of the host insect [START_REF] Fan | Can't take the heat: high temperature depletes bacterial endosymbionts of ants[END_REF][START_REF] Kikuchi | Collapse of insect gut symbiosis under simulated climate change[END_REF]. For example, EHTs decrease the quantity of symbiotic bacteria, lowering heat tolerance in ants [START_REF] Fan | Can't take the heat: high temperature depletes bacterial endosymbionts of ants[END_REF] and aphid species (142), and altering fitness-related traits in stinkbugs [START_REF] Kikuchi | Collapse of insect gut symbiosis under simulated climate change[END_REF]. Nevertheless, endosymbiosis may assist insect hosts to adapt to natural EHTs. In aphids, clones with heat tolerant symbionts develop faster than clones without under EHTs [START_REF] Harmon | Species response to environmental change: impacts of food web interactions and evolution[END_REF]. Mutants of the symbiont Buchnera aphidicola with lower expression of heat-shock gene ibpA decrease heat tolerance of pea aphids (142). In addition, facultative symbionts, e.g.

Serratia symbiotica and Acetobacter can protect B. aphidicola from short-term heat shock, improving aphid fecundity and offspring survival under EHTs (100).

Morphological responses

EHTs can induce changes in body size of insects. High developmental temperature generally produces small individuals due to enhanced metabolism and fast development [START_REF] Atkinson | Temperature and organism size: a biological law for ectotherms?[END_REF][START_REF] Caradonna | Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change[END_REF]131). This temperature-size rule arises due to phenotypic plasticity or selection for smaller body sizes [START_REF] Atkinson | Temperature and organism size: a biological law for ectotherms?[END_REF][START_REF] Forster | Warming-induced reductions in body size are greater in aquatic than terrestrial species[END_REF], although smaller individuals are more vulnerable to dehydration and overheating [START_REF] Gardner | Declining body size: A third universal response to warming?[END_REF]. However, small body size may facilitate heat damage in insect gut or gut symbionts, depriving nutrients and water [START_REF] Kikuchi | Collapse of insect gut symbiosis under simulated climate change[END_REF]. However, we know little about the growth trajectories under repeated EHTs and the underlying physiological mechanisms. For example, frequent heat exposure produces large individuals sometimes(123, 140). The selective advantage of smaller size might become disadvantageous under repeated EHTs (44).

Fitness-related life history traits and demography

Stage-specific responses

All stages of insects may experience EHTs. Meanwhile, different stages or instars often have different thermal sensitivities [START_REF] Bowler | Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?[END_REF][START_REF] Kingsolver | Complex life cycles and the responses of insects to climate change[END_REF]146). Therefore, EHTs may produce stage-specific thermal responses. Generally, the thermal response of development, survival, reproduction and longevity varies with life stage (144) and adults are often more vulnerable to EHTs. For example, EHTs reduced more reproduction when they occurred closer to adulthood (141, 143). Both early and reproductive stages of Sitobion avenae (146) and Plutella xylostella (143) are the most sensitive to EHTs compared to mature larvae. Thus, the stage at which the insects are exposed to EHTs is an important component setting the impact of EHTs. Three potential mechanisms may be involved in ontogenetic variations of thermal tolerance. 1) "Microclimate selection" hypothesis states that different stages live in and thus adapt to different thermal environments [START_REF] Kingsolver | Complex life cycles and the responses of insects to climate change[END_REF]108,139). 2) "Body size" hypothesis (75) explains why larger larvae are more heat tolerant than the smaller early life stages (86,144,146) which have faster increase of body temperature (3) and water loss [START_REF] Gibbs | Effects of temperature on cuticular lipids and water balance in a desert Drosophila: is thermal acclimation beneficial?[END_REF], but it fails to explain the decreased tolerance at adult stage. 3) "Bogert effect" hypothesis suggests that the immobile stages (egg and pupa) should be more heat tolerant than mobile adult and larval stages due to their lower ability for behavioral thermoregulation [START_REF] Huey | Behavioral drive versus behavioral inertia in evolution: a null model approach[END_REF], but this hypothesis has been rejected frequently [START_REF] Klockmann | Heat resistance throughout ontogeny: body size constrains thermal tolerance[END_REF].

Trait-dependent responses

Different life history traits differ in their thermal sensitivity [START_REF] Kellermann | Terrestrial insects and climate change: adaptive responses in key traits[END_REF]. Among the main life history traits, reproduction has the narrowest thermal range, followed by development, while survival has the widest. Reproductive potential is expected to be the most vulnerable fitness-related life history traits to EHTs (136, 143). For example, a single hot event of few hours does not affect survival but decreases reproduction in the moths Plutella xylostella (145) and Grapholitha molesta [START_REF] Liang | A single hot event stimulates adult performance but reduces egg survival in the oriental fruit moth, Grapholitha molesta[END_REF]. The optimal temperature for reproduction is lower than for development (89, 147), while the optimal temperature for immature survival is often a relatively wide range. When temperature increases continuously and surpasses the optimum, development would be restricted and soon mortality occurs [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF][START_REF] Karl | Temperature extremes and butterfly fitness: conflicting evidence from life history and immune function[END_REF]89), indicating slightly higher temperature thresholds for survival than for development. Thus, the critical upper thermal limits are: reproduction < development < survival (89, 147).

Immediate, cross-stage and transgenerational responses

The impact of EHTs occurs at various temporal scales across insect life cycles, leading to immediate impacts at the exposed stage [START_REF] Chen | More stressful event does not always depress subsequent life performance[END_REF]86,116,140), permanent damage at later stages through carry-over effects [START_REF] Chen | More stressful event does not always depress subsequent life performance[END_REF][START_REF] Klockmann | Heat resistance throughout ontogeny: body size constrains thermal tolerance[END_REF]141,144,146), and transgenerational effects via parental effects (145). The immediate impacts incur all the molecular, physiological, and morphological mechanisms developed above and are reflected in heat death or delayed development during the events. EHTs in early life stages can influence performance of later stages or next generation depending on the intensity of EHTs, although this is still a matter of debate. Lifecycle modularity hypothesis and adaptive decoupling hypothesis (116) state that early life stress has no effects on adult performance, probably because the stressful temperatures are not extreme enough. However, there is evidence that extreme temperatures occurring in egg, larval or pupal stages can decrease survival (144) and fecundity [START_REF] Chen | More stressful event does not always depress subsequent life performance[END_REF][START_REF] Klockmann | Heat resistance throughout ontogeny: body size constrains thermal tolerance[END_REF]141,146) of adults through carry-over effects, or even result in decreased offspring survival via transgenerational effects (145). Nevertheless, we still know little about the mechanisms underlying carry-over and transgenerational effects of extremes.

Population dynamics

Phenology and voltinism

Frequent EHTs increase overall mean temperature, advancing spring and postponing autumn in the calendar, and causing shorter winters and longer growing seasons (99).

For non-diapausing insects, frequent EHTs may advance phenology in spring and postpone phenology in autumn, increasing thereby the number of annual generations (2, 99). However, for insects with obligate diapause, the combination of longer summers and shorter/warmer winters delays adult emergence due to insufficient winter chilling for diapause termination and to the reduced ability to regulate the onset and termination of diapause [START_REF] Caradonna | Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change[END_REF]. For insects with facultative diapause, winter warming leads to earlier diapause termination (127). Nevertheless, EHTs do not always significantly increase the overall mean temperature and their effects on phenology and voltinism remain largely unknown for most insects. Few consecutive hot days occurring in autumn or spring would potentially disturb diapause induction or post-diapause development, thereby altering the phenology of insects.

Abundance

Repeated EHTs generally depress insect survival, fecundity and abundance [START_REF] Caradonna | Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change[END_REF]87,89,101,122,147). For example, the increase in daily maximum temperature dramatically reduces arthropod biomass in a rainforest [START_REF] Lister | Climate-driven declines in arthropod abundance restructure a rainforest food web[END_REF]. However, the effects of EHTs on insect abundance are complex due to the variations in the characteristics of EHTs, local baseline climates and habitat uses, species-specific thermal sensitivity of insects and the biotic interactions with other species. For instance, frequent EHTs depress abundance of heat sensitive species Sitobion avenae and Schizaphis graminum whereas they have null or even positive impacts on the heat tolerant species Ropalosiphum padi (92). Frequent EHTs reduce the abundance of S. avenae at the southern margin but not in the north (92). EHTs may also favor soil insects by enhancing their reproduction and abundance [START_REF] Lindo | Warming favours small-bodied organisms through enhanced reproduction and compositional shifts in belowground systems[END_REF]. Extremely warm winters occurring at high latitudes can increase insect abundance [START_REF] Goodsman | The effect of warmer winters on the demography of an outbreak insect is hidden by intraspecific competition[END_REF]. However, EHTs in the Arctic winter also accelerate snowmelt, decreasing indirectly insect abundance [START_REF] Bokhorst | Extreme winter warming events more negatively impact small rather than large soil fauna: shift in community composition explained by traits not taxa[END_REF].

Biotic interactions and community structure

Changes in community composition and structure

Differences in thermal tolerance of insects at the same trophic level can alter the relative dominance and interspecific competition among species [START_REF] Bokhorst | Extreme winter warming events more negatively impact small rather than large soil fauna: shift in community composition explained by traits not taxa[END_REF][START_REF] Cerda | The role of competition by dominants and temperature in the foraging of subordinate species in Mediterranean ant communities[END_REF][START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF]92), leading to EHT-driven changes in the composition of communities (130). For example, more frequent EHTs alter the structure of cereal aphid communities across large temporal and geographical scales (92). In this case, EHTs alter the dominant pest species in winter wheat crops (92). EHT during summer affects interspecific competition in Mediterranean ant communities by changing the circadian rhythm of foraging in subdominant ants but not for dominant species [START_REF] Cerda | The role of competition by dominants and temperature in the foraging of subordinate species in Mediterranean ant communities[END_REF]. Insects are usually at the intermediate or lower trophic levels in communities and ecosystems. The EHT-induced changes in the composition and structure of insect communities could potentially influence top-down and bottom-up processes in plant-insect herbivore-predator systems.

Cascading effects across multitrophic systems

Increasing frequency and intensity of EHTs enhances vulnerability of species at higher trophic levels [START_REF] Chen | Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level[END_REF]101), although this rule cannot be generalized [START_REF] Franken | Heated communities: Large inter-and intraspecific variation in heat tolerance across trophic levels of a soil arthropod community[END_REF]122).

Thus, EHTs are likely to reduce predator diversity and disrupt ecosystem services such as natural biological control [START_REF] Barton | Experimental warming transforms multiple predator effects in a grassland food web[END_REF]. Nevertheless, biodiverse multi-trophic assemblages are more resilient to EHTs [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF][START_REF] Isbell | Biodiversity increases the resistance of ecosystem productivity to climate extremes[END_REF]122). For simplified food-chains including only two trophic levels such as plant-insect herbivore [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF], prey-predator (101, 122) or parasitoid-hyperparasitoid systems [START_REF] Chen | Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level[END_REF], the species at higher trophic levels are more susceptible to EHTs. However, the overall effects of EHTs on tri-trophic systems such as plant-insect herbivore-predator/parasitoid are much less dramatic and often similar to patterns under normal climates [START_REF] Gillespie | Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species[END_REF]122). Studies on the relationship between EHTs and the responses of each trophic level are helpful to clarify the resilience of ecological communities to changes in climate extremes.

Geographical distributions

Heat tolerance is weakly linked to latitude in insects, but tolerant species often are in warm microhabitats while heat vulnerable species remain mostly in cooler microhabitats [START_REF] Franken | Heated communities: Large inter-and intraspecific variation in heat tolerance across trophic levels of a soil arthropod community[END_REF]110). Thermal safety margin, defined as the difference between the CTmax of insects and the ambient maximum temperature of the hottest month [START_REF] Kellermann | Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically[END_REF]134), is frequently used to predict insect distribution following EHTs. Thermal extremes exceeding CTmax restrict the thermal performance range and influence the distribution across latitudes and altitudes and in heterogeneous landscapes [START_REF] Kingsolver | Heat stress and the fitness consequences of climate change for terrestrial ectotherms[END_REF]104,134), shaping thereby the distribution of insects worldwide [START_REF] Kellermann | Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically[END_REF]94). EHTs can shift distributions through local extinction induced by mass mortality due to fitness decline, to mismatch in the phenology of insects and host plants [START_REF] Caradonna | Experimental warming in the field delays phenology and reduces body mass, fat content and survival: Implications for the persistence of a pollinator under climate change[END_REF]97) or to interaction with landscape fragmentation (106). However, EHTs in winter or nighttime may release the constraint of low temperatures, leading to positive effects such as increased winter survival and dispersal abilities in insects [START_REF] Battisti | A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly[END_REF][START_REF] Battisti | Expansion of geographic range in the pine processionary moth caused by increased winter temperatures[END_REF], resulting in range expansion.

Prolonged heat waves lead to an increase in number of nights above the flight threshold temperature, promoting the take-off behavior in Thaumetopoea pityocampa and causing a rapid distribution shift to higher altitudes in the Alps (9). Some species with higher adaptive potential in heat tolerance can expand their range to lower latitudes [START_REF] Hill | A predicted niche shift corresponds with increased thermal resistance in an invasive mite, Halotydeus destructor[END_REF].

HOW DO INSECTS BUFFER AGAINST THERMAL EXTREMES?

Microhabitats as filters of thermal extremes

Mosaic of microclimates

Forecasting biological impacts of EHTs requires general understanding how microhabitats filter environmental fluctuations and whether the heterogeneity will allow insects to escape heat extremes [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]113,129). Living and non-living objects in the environment produce a complex mosaic of microclimates which depends on the nature of the objects and how the microhabitat transfers atmospheric variations (138).

Little is known, however, on the dynamics of these microclimatic mosaics during thermal extremes (111). In the apple tentiform leaf miner, the location within the tree canopy mosaic of optimal, sub-optimal and lethal micro-environments can be totally reversed during EHTs (112). The temperature gradient at micro-scale matters much for arthropods to escape EHTs. For example, in the flat-rock spider in Australia, few centimeters below hot rocks are enough to change the temperature by 9°C (107).

Similarly, the temperature heterogeneity on surface of leaves can be 6 to 12°C (121).

Spider mites can fully exploit this heterogeneity by moving over few centimeters but this possibility is restricted during EHTs [START_REF] Caillon | Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods[END_REF]. Aphids are more constrained for their feeding behavior and cannot really exploit this heterogeneity [START_REF] Cahon | Do aphids alter leaf surface temperature patterns during early infestation?[END_REF]. EHTs are expected to alter these fine-scale temperature gradients [START_REF] Caillon | Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods[END_REF], depending on the baseline buffering property of the microhabitat (138).

Buffering ability of microhabitats

EHTs are transmitted through microhabitat before they reach insects. Different microhabitats filter atmospheric conditions differently. For example, differences of >5°C in the maximal microclimate temperature were measured when comparing different habitats e.g. grassland, heathland and deciduous woodland (128). The understory of forests is probably the strongest buffer of EHTs [START_REF] De Frenne | Microclimate moderates plant responses to macroclimate warming[END_REF], which is almost independent of the dominant tree species and of latitude [START_REF] De Frenne | Global buffering of temperatures under forest canopies[END_REF]. Insects would benefit from moving to these microhabitats during EHTs although a direct effect remains to be demonstrated. Nevertheless, some insect species are specialized to microhabitats at the top canopy and the potential for vertical zonation of herbivore insects across forest canopies is important [START_REF] Lawton | Plant architecture and the diversity of phytophagous insects[END_REF]. The temperature of leaves hit by solar radiation is higher than ambient air temperature in temperate and boreal latitudes (113), thus the leaf surface magnifies the amplitude of thermal extremes (138). The thermal limit of small herbivore arthropods living at the leaf surface is related to leaf temperature during EHTs (110). Therefore, these herbivores are already vulnerable to contemporary thermal extremes. Similarly, endophagous insects such as leaf miners and gall-inducing organisms are living in their structures (mines, galls) where temperature increases more than ambient air during thermal extremes (108, 109). By contrast, aquatic systems buffer atmospheric temperature variations due to the thermal inertia of water bodies and geophysical processes (138). In general, we lack data on the temperature of most microhabitats to provide an exhaustive ranking from the best to the worse buffer of EHTs.

Thermoregulation

Behavioral thermoregulation across the mosaic of microclimates plays an important role in avoiding EHTs (95). Thermoregulatory behavior can directly increase survival during EHTs [START_REF] Bonebrake | From global change to a butterfly flapping: biophysics and behaviour affect tropical climate change impacts[END_REF][START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]138). Nevertheless, the availability of suitable microclimates is needed for thermoregulation (138), determining the efficacy of insect buffering against climate warming [START_REF] Caillon | Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods[END_REF][START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]. However, it is predicted that warming will reduce seasonal and diurnal temperature ranges [START_REF]Summary for policymakers[END_REF], causing decreases in temperature heterogeneity across temporal and spatial scales [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF] including microhabitats [START_REF] Caillon | Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods[END_REF].

Thus, behavioral thermoregulation alone may not be sufficient to buffer ongoing climate warming [START_REF] Caillon | Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods[END_REF].

Behavioral thermoregulation can also bring costs and lead to ecological consequences.. More frequent EHTs increase occurrence of thermoregulatory behaviors (90, 137) and maintenance energy costs [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF], and in turn decrease foraging activity, energy efficiency and reproduction [START_REF] Kearney | The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming[END_REF]87). For example, aphids leave their host plants by dropping off or walking downward to seek cooler microhabitats to escape EHTs (86, 90, 91, 102). Therefore, they may have to endure food and water deprivation and spend time and energy to find another suitable feeding site, thereby reducing reproduction opportunities (88). Moreover, behavioral thermoregulation may also alter the microhabitat use of insects [START_REF] Barton | Experimental warming transforms multiple predator effects in a grassland food web[END_REF]88). Differences in behavioral regulations and microhabitat use between species can change interspecific interaction and food web structure [START_REF] Barton | Experimental warming transforms multiple predator effects in a grassland food web[END_REF]. Furthermore, thermoregulatory behavior may limit evolutionary adaptation by reducing or even eliminating the selection pressure of EHTs (58).

Ontogenetic variations and tradeoff between different traits

Insects evolved complex life cycles with multiple developmental stages differing in thermal sensitivity [START_REF] Bowler | Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?[END_REF]. However, the role of ontogenetic variation of thermal sensitivity in buffering EHTs has received little attention. Different stages/age cohorts can overlap in field populations, resulting in the coexistence of multiple life stages/age cohorts during growth season. When the mixed-stage population experiences EHTs, the most sensitive stages would be injured or die whereas the most tolerant may survive and develop to adult stage for reproduction during the following mild phases, thereby contributing to population recovery. Comparing to pupal and adult stage, medium and late larval stage can particularly resist heat stress in both immediate survival and subsequent reproduction (145) Larval stages may acquire sufficient nutrients and water to both resist EHTs and provide enough time to recover from heat injury, reducing thereby the carry-over effects of EHTs on adult reproduction.

The intrinsic rate of increase, a metric for fitness, integrates survival, development time and reproduction (87, 89). Different responses to EHTs and even trade-off between these traits may also help buffer impacts of EHTs. Temperatures above the optimum for reproduction reduce fecundity (eg, number of offspring) but can also accelerate maturation and reproduction processes (143, 147). Then, when temperature surpasses the optimum for development, insects tend to invest more energy in heat tolerance to improve survival, generating costs that reduce reproduction output (146) and delay development at least temporally (116, 140). Thus, variations in thermal sensitivity of different traits may contribute to buffer heat stress in insects.

Phenotypic plasticity

Phenotypic plasticity is a non-genetic strategy to cope with environmental variation including thermal extremes [START_REF] Gunderson | Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming[END_REF][START_REF] Hoffmann | Upper thermal limits in terrestrial ectotherms: how constrained are they?[END_REF]133). Most of the insect responses detailed above relate to phenotypic plasticity. Four types of plasticity in heat tolerance were identified based on the time scale and temperature intensity. "Rapid hardening/heat shock" corresponds to a short and harsh exposure to high temperature for a few minutes or hours [START_REF] Kellermann | How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster[END_REF]133). The other types of thermal plasticity are all generated by exposure to moderately high temperatures for several hours to days for "acclimation" (laboratory) or "acclimatization" (field) [START_REF] Jensen | Thermal acclimation and adaptation across populations in a broadly distributed soil arthropod[END_REF][START_REF] Kellermann | How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster[END_REF], days to weeks for "development acclimation/plasticity" [START_REF] Kellermann | Evidence for lower plasticity in CTMAX at warmer developmental temperatures[END_REF][START_REF] Kellermann | How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster[END_REF]133) and weeks to months for "transgenerational acclimation" [START_REF] Jensen | Thermal acclimation and adaptation across populations in a broadly distributed soil arthropod[END_REF]. In general, previous exposure to elevated temperatures increases heat tolerance both within and across generations.

Nevertheless, the potential to buffer against EHTs through plasticity may be limited. Quantitatively, there is limited scope for plasticity to increase heat tolerance significantly in many arthropod taxa [START_REF] Gunderson | Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming[END_REF][START_REF] Hoffmann | Upper thermal limits in terrestrial ectotherms: how constrained are they?[END_REF][START_REF] Kellermann | Evidence for lower plasticity in CTMAX at warmer developmental temperatures[END_REF]133). For instance, the increases in CTmax of some Drosophila species and the moth Manduca sexta are limited to only 0.6~1.0 °C [START_REF] Kellermann | Evidence for lower plasticity in CTMAX at warmer developmental temperatures[END_REF]133) and 1~2 °C [START_REF] Kingsolver | Plasticity of upper thermal limits to acute and chronic temperature variation in Manduca sexta larvae[END_REF], respectively, via hardening and developmental acclimation processes. In addition, increased heat tolerance brings a series of concurrent costs in other plastic traits that are related to fitness [START_REF] Esperk | Plastic and evolutionary responses to heat stress in a temperate dung fly: negative correlation between basal and induced heat tolerance?[END_REF][START_REF] Loeschcke | Consequences of heat hardening on a field fitness component in Drosophila depend on environmental temperature[END_REF]133). These costs can generate considerable transgenerational consequences such as declined offspring size and survival (93).

Evolutionary adaptation

Frequent EHTs could induce evolution of thermal tolerance to buffer against high temperature impacts (16, 57). Thermal evolution occurs in small insects during artificial selections [START_REF] Folk | Selection on knockdown performance in Drosophila melanogaster impacts thermotolerance and heat-shock response differently in females and males[END_REF][START_REF] Hangartner | Evolutionary potential of multiple measures of upper thermal tolerance in Drosophila melanogaster[END_REF]. Long-term thermal selection is commonly found in local adaption, e.g. drosophila and ants at different latitudes [START_REF] Diamond | Evolutionary potential of upper thermal tolerance: biogeographic patterns and expectations under climate change[END_REF]104), or beetles and butterflies at different altitudes [START_REF] Garcí A-Robledo | Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction[END_REF][START_REF] Higgins | Geographic differences and microevolutionary changes in thermal sensitivity of butterfly larvae in response to climate[END_REF]. Urban heat island also triggers thermal adaptation. Urban workers of ants evolved a CTmax 1°C higher than the rural populations [START_REF] Diamond | Evolutionary potential of upper thermal tolerance: biogeographic patterns and expectations under climate change[END_REF]. Local adaptation often results from a subtle interaction between generation time, heritability, covariance between phenotypes, phylogenetic inertia and the strength of selection [START_REF] Kellermann | Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically[END_REF].

However, rapid evolution of thermal traits hardly occurs under natural selection in insects. Higher feeding rates evolved only after decades in nature under more frequent EHTs in Colias eurytheme [START_REF] Higgins | Geographic differences and microevolutionary changes in thermal sensitivity of butterfly larvae in response to climate[END_REF]. EHTs imbedded in fluctuating patterns may constrain the evolution of thermal traits due to lower heritability under ramping temperature than artificial static temperature (98), slowing down the speed at which insects can track climate warming [START_REF] Hangartner | Evolutionary potential of multiple measures of upper thermal tolerance in Drosophila melanogaster[END_REF]. Thermal selection can also modify fitness-related life history traits [START_REF] Huey | Evolution of thermal sensitivity of ectotherm performance[END_REF][START_REF] Kingsolver | Quantifying thermal extremes and biological variation to predict evolutionary responses to changing climate[END_REF]. Thermal tolerance often incurs fitness costs due to antagonistic genetic interactions between traits [START_REF] Loeschcke | Selection for heat-shock resistance in larval and in adult Drosophila buzzatii: comparing direct and indirect responses[END_REF]. Thermal tolerance could also be shaped by phylogenetic inertia rather than thermal selection in nature [START_REF] Kellermann | Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically[END_REF]. To some extent, thermal evolution can be a way to buffer EHTs, but its mechanisms are still evasive.

KNOWLEDGE GAP AND FUTURE PERSPECTIVES

Ecological relevance of experimental designs

The biological impacts of complex EHTs are difficult to investigate experimentally because of their stochastic nature. Open top chambers, infrared irradiation and electronic heating systems are widely used to simulate climate warming including EHTs in the field [START_REF] Halbritter | The handbook for standardized field and laboratory measurements in terrestrial climate change experiments and observational studies (ClimEx)[END_REF]. However, results from these studies are difficult to apply broadly because the mechanisms are not fully understood. The different statistical moments of EHTs (intensity, duration, and frequency) may have biological impacts differing in their direction and amplitude, and their interactive effects could generate counter-intuitive responses in insects. Simulated regimes of EHTs are highly diverse in the literature, including constant temperature for given periods or fluctuations with fixed cycles. Currently, these regimes do not include alternative patterns of EHTs and mild periods which allow stress recovery (87, 147).

Here we call for experimental designs with enhanced ecological relevance in future studies by incorporating the complete statistics of EHTs despite the inherent logistic complexity of factoring several variables. In addition, the simulated temperature regimes should be based on microclimatic rather than macroclimatic patterns to improve the ecological relevance. Such level of complexity is mandatory to help us to draw the landscape of insect performances under EHTs in natural thermal conditions.

Enlarging our vision of extremes

EHTs are by climatological definition relatively infrequent but intense (eg, heat waves). The biological perspective is more conservative in the sense that the thermal events challenging the physiology of insects are likely frequent. Environmental conditions may become suddenly challenging for organisms when several normal events co-occur leading to environmental extremes [START_REF] Denny | On the prediction of extreme ecological events[END_REF]. This shift in perspective was only rarely applied to insects but the methodology and the concepts exist [START_REF] Dowd | A series of unfortunate events: characterizing the contingent nature of physiological extremes using long-term environmental records[END_REF]. Insects are constrained by several factors in their microhabitats. Dryness aggravates the physiological stress during hot periods. Wind decreases body temperature in the short term, but it incurs higher water loss. The same set of environmental conditions may be extreme for individuals deprived of appropriate endosymbionts but near optimal for those that host these microorganisms. Entomological sciences need to embrace more original and innovative characterizations of extreme events, to be combined with the standard climatological view.

Rise of integrative approaches

The ultimate goal of global change biologists is to anticipate the future trend of biodiversity. This goal can only be achieved by comprehensive understanding of the mechanisms for organism-environment interactions, and predicting population dynamics and community structure across time/generations. It seems crucial to link physiological mechanisms of thermal stress and the demographic variables.

Physiological and genomic approaches have been successfully integrated in studies to link physiological impacts of environmental changes and field patterns of thermal stress. Intertidal ecologists probably led this vision for decades [START_REF] Helmuth | Biophysics, physiological ecology, and climate change: Does mechanism matter?[END_REF], but entomologists now are aligned [START_REF] Giron | Promises and challenges in insect-plant interactions[END_REF]. The next challenge is to integrate the 'field ecophysiology' of thermal stress, especially during EHTs, and the population dynamics. Given the importance of individual processes (e.g., carry-over effects, hardening of thermal tolerance, and more generally phenotypic plasticity), approaches including individual-based models [START_REF] Crespo-Pé Rez | Changes in the distribution of multispecies pest assemblages affect levels of crop damage in warming tropical Andes[END_REF] are promising candidates to interconnect these processes and link individual and population scales. In addition, microclimate models are needed [START_REF] Kearney | NicheMapR -an R package for biophysical modelling: the microclimate model[END_REF]111,112) to simulate the heterogeneous environmental arena within which individuals and species are interacting. Nevertheless, all these processes need to be fine-scaled to incorporate cross-seasonal impacts of EHTs at given moment in the life cycle of insects. Intense collaborations between physiologists, ecologists, climatologists and modelers are key for successful developments.

CONCLUDING REMARKS

Thermal extremes are complex events that combine different statistical moments. This complexity adds up the difficulty of getting a comprehensive understanding of their impacts on biological processes. While thermal extremes are defined as rare events by climatologists, ecologists realized that thermal extremes are much more frequent once they are defined relative to the thermal biology of organisms.

Nevertheless, the impacts of ongoing climate change on these "biologically-relevant thermal extremes" remain to be identified. In this context, the most studied biological models are Drosophila species [START_REF] Feder | Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae[END_REF][START_REF] Hangartner | Evolutionary potential of multiple measures of upper thermal tolerance in Drosophila melanogaster[END_REF][START_REF] Kellermann | Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically[END_REF] and other species with conservation importance [START_REF] Isbell | Biodiversity increases the resistance of ecosystem productivity to climate extremes[END_REF][START_REF] Lister | Climate-driven declines in arthropod abundance restructure a rainforest food web[END_REF]. The thermal ecology of most species with economic importance for agriculture, horticulture and forestry remains largely unknown. Extreme absence of knowledge is an important frontier limiting our ability to anticipate the ecological consequences of extreme heat events.

535

SUMMARY POINTS

1. Thermal extremes are complex, multicomposite events. Despite a lack of unified definition of thermal extremes due to this complexity, we can describe natural temperature extremes with several variables related to both the environment and the species thermal biology, defining together the intensity, frequency and temporal variance of extreme high temperature events. 2. Classic thermal performance curves (TPCs) derived from constant temperature experiments cannot be used to estimate the biological impacts of thermal extremes. More sophisticated TPCs are needed to include the influence of the all statistical moments of thermal extremes. 3. Extreme high temperatures often, but not always affect insects at various levels, ranging from molecular and physiological responses, at individual to population scales, to community structure and functioning.

4. Thermal extremes can affect instantaneously survival. They can also produce long-lasting impacts on life history traits and demographics of insects. The magnitude of these effects depends mainly on thermal history, traits and life-cycle stage. Collectively, all these effects translate into population dynamics. 5. Insects may buffer partly or completely the thermal extremes via behavioral thermoregulation, phenotypic plasticity, ontogeny variations, trade-off between different traits and evolutionary adaptation. However, most of these buffering strategies probably have limited potential quantitatively, and they may incur costs for other fitness-related traits.

FUTURE ISSUES

1. Innovative, ecologically-relevant experimental designs are crucially needed to better understand the effects of realistic natural thermal extremes on insect populations, communities and ecosystems.

2. Beyond the instantaneous impacts of thermal extremes, the carry-over effects of heat stress and the stage-specific responses of insects deserve more comprehensive studies to better detail the consequences of thermal extremes. 3. We lack studies on the relative effects of the various strategies to buffer against thermal extremes, including physiological and behavioral thermoregulation, ontogenetic variation, phenotypic plasticity and adaptive evolution in insects. These buffering strategies may incur trade-offs with fitness-related traits, generating complex interactive effects that need to be identified to feed prediction models. 4. The mechanisms underlying heat injury and thermal recovery of insects at the molecular, physiological and ecological levels should be revealed to better comprehend the combined effects of alternating thermal extremes and mild periods. 5. The impacts of extreme high temperatures occurring in fall, winter and spring as well as at night on insect diapause, phenology, interspecific interactions and communities remain relatively understudied.

6. Microclimate models should be used more extensively to generate realistic thermal environments within which insects experience thermal extremes under field conditions in their microhabitats. 7. The thermal biology in context of thermal extremes of insect species of economic importance such as agricultural, horticultural and forestry pests, and their potential biological control agents, should be given priority to improve pest management and beneficial conservation worldwide.

  apple maggot Rhagoletis pomonella during hot summer days and overwintering diapause. Physiol. Entomol. 33:346-52 86. Ma CS, Hau B. Poehling HM. 2004. The effect of heat stress on the survival of the rose grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae). Eur. J. Entomol. 101:327-31 87. Ma CS, Wang L, Zhang W, Rudolf V. 2018. Resolving biological impacts of multiple heat waves: interaction of hot and recovery days. Oikos 127:622-33 88. Ma G, Bai CM, Wang XJ, Majeed MZ, Ma CS. 2018. Behavioural thermoregulation alters microhabitat utilization and demographic rates in ectothermic invertebrates. Anim. Behav. 142:49-57 89. Ma G, Hoffmann AA, Ma CS. 2015. Daily temperature extremes play an important role in predicting thermal effects. J. Exp. Biol. 218:2289-96 90. Ma G, Ma CS. 2012. Climate warming may increase aphids' dropping probabilities in response to high temperatures. J. Insect Physiol. 58:1456-62 91. Ma G, Ma CS. 2012. Effect of acclimation on heat-escape temperatures of two aphid species: implications for estimating behavioral response of insect to climate warming. J. Insect Physiol. 58:303-309 92. Ma G, Rudolf V, Ma CS. 2015. Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob. Change Biol. 21:1794-1808 93. Macagno ALM, Zattara EE, Ezeakudo O, Moczek AP, Ledonrettig C. 2018. Adaptive maternal behavioral plasticity and developmental programming mitigate the transgenerational effects of temperature in dung beetles. Oikos 127:1319-29 94. Martinet B, Lecocq T, Smet J, Rasmont P. 2015. A protocol to assess insect resistance to heat waves, applied to bumblebees (Bombus Latreille, 1802). PLoS ONE 10:e0118591 95. May ML. 1979. Insect thermoregulation. Annu. Rev. Entomol. 24:313-49 96. Meehl G A, Tebaldi C. 2004. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994-97 97. Merrill RM, Gutierrez D, Lewis OT, Gutierrez J, Diez SB, Wilson RJ. 2008. Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. J. Anim. Ecol. 77:145-55 98. Mitchell KA, Hoffmann AA. 2010. Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila. Funct. Ecol. 24:694-700 99. Mitton JB, Ferrenberg SM. 2012. Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am. Nat. 179:163-71

Figure captions Figure 1 .

 captions1 Figure captions

Figure 2 .

 2 Figure 2. Characterizing Extreme High Temperatures (EHTs) in the field. (a) A

Figure 2

 2 Figure 2

ACKNOWLEDGMENTS

The work was supported by research grants of National Natural Science Foundation of China (31620103914 and 31772156) and National key R & D Program of China

DISCLOSURE STATEMTNT

The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

Here, the temporal arrangement of hot and mild days varies across two axis defined by number of hot days during a period of 10 days (frequency) and the variance in the number of mild days between each hot day (temporal variance). Note that in panel d, the global mean and variance of temperature remain the same across all configurations at a given frequency of hot days.