BACKGROUND: Climate warming is considered to affect the characteristics of heat waves by increasing their duration, frequency and intensity, which can have dramatic consequences for ectothermic arthropods. However, arthropods may respond to heat waves via plastic modifications, which could differently affect a predator and its prey. We examined this assumption using prominent counterparts in biological control, the predatory mite Phytoseiulus persimilis and its prey, the spider mite Tetranychus urticae . Individuals of both species were separately exposed to mild and extreme heat waves during their juvenile development. RESULTS: Both species developed faster during extreme heat waves, but the proportional increase of the developmental rates was higher in the prey. Independent of sex, P. persimilis reached smaller size at maturity under extreme heat waves, whereas the body size modifications were sex‐dependent in T. urticae : males became smaller, but females were able to maintain their size. CONCLUSIONS: An accelerated development may result in the reduction of the exposure time of susceptible juvenile stages to heat waves and prey stages to predators. Plastic size adjustments caused a shift in the female predator–prey body size ratio in favor of the prey, which may lead to higher heat resistance and reduced predation risk for prey females under extreme heat waves. In conclusion, our findings indicate that species‐specific shifts in age and size at maturity may result in lower suppression efficacy of the predator P. persimilis against its prey T. urticae with severe consequences for biological control of spider mites, if global warming continues.

The thermal history of arthropod predators and their prey may affect their reproductive performance during heat waves. Thus, a matching juvenile and adult environment should be beneficial as it enables the individuals to acclimate to extreme conditions. Prey fecundity, however, is also affected by a second stressor, namely predation risk. Here, we assessed the impact of extreme and mild heat waves on the reproductive output of acclimated (juvenile and adult heat wave conditions are matching) and non-acclimated females of the biocontrol agent Phytoseiulus persimilis, a predatory mite, and its herbivorous prey, the two-spotted spider mite Tetranychus urticae, on bean leaves. Their escape and oviposition rates and egg sizes were recorded over 10 days. Additionally, ovipositing prey females were exposed to predator cues and heat waves. Acclimation changed the escape rates and egg sizes of both species, whereas fecundity was only influenced by the adult thermal environment via increased egg numbers under extreme heat waves. Acclimation reduced predator and prey escape rates, which were higher for the predator. Pooled over acclimation, both species deposited more but smaller eggs under extreme heat waves. Acclimation dampened this effect in prey eggs, whereas acclimation resulted in smaller female eggs of the predator. Prey deposited larger male and female eggs. Predator cues reduced prey oviposition, but the effect was small compared to the large increase gained under extreme heat waves. We argue that the success of predators in controlling spider mites during heat waves mainly depends on the fates of escaping predators. A permanent absence of predators may result in the numerical dominance of prey.

The more frequent and intense occurrence of heat waves is a challenge for arthropods because their unpredictable incidence requires fast adaptations by the exposed individuals. Phenotypic plasticity within and across generations might be a solution to cope with the detrimental effects of heat waves, especially for fast‐developing, small arthropods with limited dispersal abilities. Therefore, we studied whether severe heat may affect the reproduction of a pest species, the spider mite Tetranychus urticae, and its counterpart, the predatory mite Phytoseiulus persimilis. Single offspring females with different parental thermal origins (reared under mild or extreme heat waves) of both species were exposed to mild or extreme heat waves on bean leaves over 10 days, and the oviposition, egg sizes, survival, and escape behavior of the females were evaluated daily. The total losses of predators mainly via escapers were very high compared to prey, which makes a separation between selective and plastic effects on shifted reproductive traits impossible. Predator females laid smaller eggs, while their consumption and oviposition rates were unaffected during extreme heat waves. In comparison, larger prey females fed more and produced more, but smaller, eggs due to within‐ and trans‐generational effects. These advantages for the prey in comparison to its predator when exposed to extreme heat waves during the reproductive phase support the trophic sensitivity hypothesis: higher trophic levels (i.e., the predator) are more sensitive to thermal stress than lower trophic levels (i.e., the prey). Furthermore, the species‐specific responses may reflect their lifestyles. The proactive and mobile predator should be selected for behavioral thermoregulation under heat waves via spatiotemporal avoidance of heat‐exposed locations rather than relying on physiological adaptations in contrast to the more sessile prey. Whether these findings also influence predator–prey interactions and their population dynamics under heat waves remains an open question.

Theoretically, parents can adjust vital offspring traits to the irregular and rapid occurrence of heat waves via developmental plasticity. However, the direction and strength of such trait modifications are often species-specific. Here, we investigated within-generational plasticity (WGP) and trans-generational plasticity (TGP) effects induced by heat waves during the offspring development of the predator Phytoseiulus persimilis and its herbivorous prey, the spider mite Tetranychus urticae, to assess plastic developmental modifications. Single offspring individuals with different parental thermal origin (reared under mild or extreme heat waves) of both species were exposed to mild or extreme heat waves until adulthood, and food consumption, age and size at maturity were recorded. The offspring traits were influenced by within-generational plasticity (WGP), trans-generational plasticity (TGP), non-plastic trans-generational effects (TGE) and/or their interactions. When exposed to extreme heat waves, both species speeded up development (exclusively WGP), consumed more (due to the fact of WGP but also to TGP in prey females and to non-plastic TGE in predator males), and predator females got smaller (non-plastic TGE and WGP), whereas prey males and females were equally sized irrespective of their origin, because TGE, WGP and TGP acted in opposite directions. The body sizes of predator males were insensitive to parental and offspring heat wave conditions. Species comparisons indicated stronger reductions in the developmental time and reduced female predator-prey body size ratios in favor of the prey under extreme heat waves. Further investigations are needed to evaluate, whether trait modifications result in lowered suppression success of the predator on its prey under heat waves or not.

Climate warming can be a powerful driver for the establishment and further spread of alien species by lowering the abiotic resistance of native ecosystems and supporting invaders. One pivotal outcome of climate warming is more frequent heat waves in summer in temperate regions. Here, we combined heat‐stress experiments (development, fecundity) and incidence data of the spotted wing drosophila (SWD), Drosophila suzukii , from two Austrian vine‐growing areas differing in their regional climate (Illyrian vs. Pannonian climate). We used corresponding climatic data (ice and hot days) and landscape elements (forests) to evaluate whether regional‐specific climate warming effects influence the distribution of SWD. Laboratory results showed that SWD is a heat‐sensitive species, with negligible survival under moderate and extreme heat waves. Under field conditions, the incidence of SWD in Austrian vineyards and the availability of surrounding forests were higher in the Illyrian than in the Pannonian climate zone. Climate warming resulted in fewer ice days in both climate zones, but the frequency of hot days has increased more strongly in the Pannonian zone over the last few decades. We conclude that forested areas near vineyards can serve as refugia both in winter and during hot summer periods. Consequently, the lower incidence of SWD in the Pannonian zone correlates with hotter summers due to climate warming and limited access to nearby forested areas. These findings highlight the urgent need for regionally tailored pest management strategies that account for the complex interplay among climate extremes, landscape features and invasive species dynamics.

Due to climate warming, predator–prey interactions involving ectothermic species will more frequently be exposed to high temperatures, and asymmetric thermal shifts of the two opponents may alter the outcome of such interactions. We observed alterations of the size at maturity in the predatory mite Phytoseiulus persimilis and its prey, the spider mite Tetranychus urticae , when separately exposed to mild or extreme heat waves during juvenile development: adult predator–prey size ratios shifted from 0.83 under mild heat waves to 0.60 under extreme heat waves. Thus, firstly, experiments were conducted under optimal temperature (25°C) to evaluate the effects of shifted body size ratios on prey survival. Second, we asked whether these asymmetric thermal alterations of the adult sizes also affect prey survival under heat. Single couples of adult predator and prey females, reared under mild or extreme heat waves, were placed on a leaf disc and exposed to mild or extreme heat (corresponding to the daily temperature peaks during juvenile development) and were videotaped for 90 min. Under optimal thermal conditions, the survival rate of prey females was highest when both species were reared under extreme heat waves, emphasizing the importance of carry‐over effects from thermal juvenile environment to adult performance. At extreme heat, prey survival was 76% compared with 42% at mild heat. The predator–prey body size ratio in favor of the prey under extreme heat wave conditions was a strong predictor of predation success. This outcome is in line with the trophic sensitivity hypothesis, stating that prey is less sensitive to heat stress than its predator. We attribute this to the fact that predators become smaller and prey larger the higher the temperature is during juvenile development. Such asymmetric thermal effects may constitute a serious obstacle for achieving successful biological control of spider mites during heat waves.