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ScienceDirect Responses of forest insect pests to climate change: not so simple Herve´ Jactel1, Julia Koricheva2 and Bastien Castagneyrol1 Climate change is a multi-faceted phenomenon, including elevated CO2, warmer temperatures, more severe droughts and more frequent storms. All these components can affect forest pests directly, or indirectly through interactions with host trees and natural enemies. Most of the responses of forest insect herbivores to climate change are expected to be positive, with shorter generation time, higher fecundity and survival, leading to increased range expansion and outbreaks. Forest insect pest can also benefit from synergistic effects of several climate change pressures, such as hotter droughts or warmer storms. However, lesser known negative effects are also likely, such as lethal effects of heat waves or thermal shocks, less palatable host tissues or more abundant parasitoids and predators. The complex interplay between abiotic stressors, host trees, insect herbivores and their natural enemies makes it very difficult to predict overall consequences of climate change on forest health. This calls for the development of process-based models to simulate pest population dynamics under climate change scenarios. Addresses 1 INRA (French National Institute for Agricultural Research), UMR 1202 BIOGECO, University of Bordeaux, 33610 Cestas, France 2 School of Biological Sciences, Royal Holloway University of London, Egham, TW20 0EX, UK Corresponding author: Jactel, Herve´ ([email protected]
Current Opinion in Insect Science 2019, 35:103–108 This review comes from a themed issue on Global change biology Edited by Arnaud Sentis and Nicolas Desneux For a complete overview see the Issue and the Editorial Available online 2nd August 2019 https://doi.org/10.1016/j.cois.2019.07.010 2214-5745/ã 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction There is a scientific consensus that Earth’s climate is changing due to increase in greenhouse gases produced by anthropogenic activities . A warmer climate may favour more mobile organisms with shorter generation www.sciencedirect.com
times as they may move and escape from harmful conditions and evolve adaptations faster than sessile species with longer generation times. Therefore, in a race to adapt to the global warming, insects are usually assumed to win over trees and signs of devastating heat effects on forests due to insect outbreaks have been reported . However, climate change involves not just raise in the temperature. Atmospheric CO2 increased from 280 to 400 ppm over the last century and may reach 550 ppm by 2050 . The frequency and intensity of extreme droughts have increased  and is predicted to increase in the future  with alarming effects on tree mortality . The same trends and predictions hold true for storm damage  whose impact on forests is exemplified by higher winter precipitations causing weaker root anchorage of trees in wetter soils . While all of the above factors can make forests more susceptible to insect pest attacks, forests have survived over geological time and the world is still green. This is because insect herbivores are regulated by bottom-up (e.g. tree defences) and top-down (e.g. predation) pressures  and both types of processes can be affected by temperatures and other climatic drivers. In this review, we reveal the complexity of the interactions between climate, forests and insects. We address the multiple and interactive dimensions of climate change effects on insect – tree interactions and provide keys to understanding the mechanisms at play in the light of the most recent publications.
Responses to temperature Predicting how global warming will affect pest damage to trees requires integrating the direct effect of increased temperatures on pest insects and its effect on their hosts and natural enemies. The relationship between temperature and developmental rate of forest insects is well known to follow a nonlinear, asymmetric curve , whereby developmental rate slowly increases between a lethal cold threshold and an optimal threshold, and then rapidly decreases until an extreme hot lethal threshold . Recent laboratory studies have additionally shown that high variability in daily temperature may reduce the survivorship of forest insects . Increased temperatures both shorten the generation time, resulting in higher voltinism, and increase the number of offspring, which might contribute to build up outbreaking populations . However, some insect species, especially those with diapause, do not reduce generation time in response to warmer temperatures (Forrester 2016). Warming can result in increased mortality, particularly in summer  as well as smaller size and lower dispersal Current Opinion in Insect Science 2019, 35:103–108
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capacity of emerging young adults . There is large latitudinal variation in thermal response among insect populations of the same species, with sometimes opposite effects at low versus high latitude margins [15,16]. Herbivores whose distribution is currently constrained by low temperatures may benefit from global warming by expanding their range . Faster herbivore development under elevated temperature generally reduces efficiency of food conversion, which herbivores compensate by increased consumption . Host tree quality (determined by primary and secondary metabolites) is also influenced by temperature [19,20]. Yet, temperature-induced changes in phytochemistry vary widely among traits and tree species. As such, the effect of increased temperature on herbivore metabolism can be exacerbated or alleviated by temperature-induced changes in tree quality. Herbivore damage can be regulated by predators and parasitoids, which are likely to be also affected by raising temperatures. Although overall positive, effects of higher temperatures on parasitoids have been found to vary greatly among endoparasitoids and ectoparasitoids as well as endophagous or ectophagous herbivore hosts . Altogether, the consequences of global warming on the damage caused by forest pests are thus very difficult to predict  as they greatly vary among insect species, notably depending on their feeding guild .
Responses to CO2 Elevated atmospheric CO2 (eCO2) generally has a negative impact on insect performance [24,25]. Most research to date has focused on indirect effects of eCO2 on insects through modification of tree traits. Generally, eCO2 causes an increase in carbohydrates, reduction in N, thus increasing C:N ratio and C-based defences that are deleterious to defoliating herbivores [26,27], with notable differences among tree species and insect functional groups [27,28]. For example, a large increase in resin flow under eCO2 might better protect pines from bark beetle attacks . Defoliators can adapt to reduced leaf nutritional quality and digestibility by increasing their consumption and metabolism [26,28], which is likely to increase herbivory under eCO2. However, at the contrary, increase in photosynthesis and carbohydrate concentrations under eCO2 could benefit phloem feeders . Studies with tree defoliators showed no significant effects of eCO2 on larval performance [30,31], but are too scarce to draw general conclusion. Direct effects of eCO2 on herbivores have received comparatively less attention. Experiments using artificial diet under ambient and eCO2 found increase in insect herbivore metabolism, reduced development time, growth and survival and increased consumption under eCO2 . This suggests that the direct effects of eCO2 on herbivores can strengthen indirect, plant-mediated effects. Current Opinion in Insect Science 2019, 35:103–108
Responses to drought Drought alters the nutritional quality of tissues consumed by herbivores , which affects herbivore performance. However, the effects of drought on tree resistance to pest insects vary depending on the feeding guild of insect herbivores . Generally, primary pests feeding on tree trunk (e.g. moths boring on pine shoot or stem) are adversely affected by drought, whereas bark beetles, leaf chewers, miners, gall makers and sap feeders benefit from drier conditions. However, these general patterns are modulated by the intensity of water stress, with usually non-linear responses . For instance, bark beetles are well known to develop outbreaks under severe droughts  whereas moderately stressed trees can be more resistant to bark beetles [35,36]. In addition to stress intensity, performance of forest insect herbivores (particularly sap-feeders) is generally higher when feeding on trees exposed to intermittent water stresses as compared to those feeding on trees exposed to constant stress (the ‘pulsed stress hypothesis’, ). Much fewer studies addressed direct effects of drought on forest insect physiology and survival, due to the difficulty of separating them from plant-mediated effects on obligatory herbivorous species. Effects of drought on higher trophic levels have been rarely studied. Not focusing on forest insect only , found neutral effect of drought on parasitoids or predators. However, recent studies showed lower parasitism rate on aphids reared on water-stressed plants due to reduced host size or abundance [39,40]. Using dummy caterpillars [41,42] observed lower predation rates by arthropods and birds in drier forests, suggesting potential indirect effects of drought on biocontrol through changes in vegetation complexity.
Responses to storms Large windthrow generally triggers outbreaks of bark beetles by providing abundant breeding substrate in the form of storm-felled or broken trees , which are unable to induce tree defences like standing healthy trees . Not surprisingly, the large recent increase in tree mortality due to bark beetle (e.g. Ips typographus, Ips sexdentatus) infestations in Europe occurred in parallel with increase in storm damage . The effects of windstorm on other forest insect herbivores are largely unknown, although a reduction in tree density following windthrow might benefit forest defoliators like the pine processionary moth . Windthrow not only produces large amount of dead or decaying wood of various sizes and species, but also forest gaps with change in microclimatic conditions, which are known to favour the abundance and diversity of saproxylic insect species , some of which are preying upon bark beetles .
Responses to interactive climatic effects Predicting effects of climate change on forest pests is especially difficult because most climatic factors co-occur and their combined effect may differ from effects of each www.sciencedirect.com
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of the climatic variables in isolation [24,26]. For instance  found additive effects of temperature and drought stress on the fitness of the scale insect Melanaspis tenebricosa on maple trees and  showed that since 1990, forest insect damages were facilitated under warmer and drier conditions. Important insights may come from studies in regions with Mediterranean climate characterized by combination of drought and hot temperatures . A number of recent empirical studies examined interactions between combinations of climatic drivers on bark beetle outbreaks and found additive, synergistic or antagonistic effects (e.g. ). Simulations with process-based models unequivocally confirm synergies between warmer temperatures and wind damage on probability of outbreaks by bark beetles [52,53]. However, interactions between windstorm and drought seem less predictable, being either neutral (i.e. additive effects, ), positive or negative . Theoretical prediction could be even trickier when considering interactions with other climate-driven pressures like snowstorms and wild fires [54,55]. Emergent studies examining three or more drivers simultaneously show an even more complex picture. For instance , found that the occurrence of large windstorms reduced the positive effect of warming
temperatures and rainfall deficit on bark beetle Ips typographus in Europe, indicating the lack of positive synergy among outbreak drivers. Using process-based models , have shown that tree mortality under the concurrent disturbance regime scenario including fire, insects, wind and forest management could be less than the sum of single disturbances, providing evidence of significant negative feedbacks among disturbance under climate change. The underlying mechanisms of interactive effects of climatic drivers on forests pests often involve changes in host plant quality. For instance, negative drought-windthrow interactions are observed in case of severe water stress directly affecting tree mortality, or drying out fallen trees, thus reducing the amount and quality of breeding substrate for bark beetles. While effects of individual climatic variables on host plant chemistry are relatively well understood, combined effects of different climatic factors often have more complex effects . For instance, a meta-analysis by  revealed that while changes in some plant chemicals such as nitrogen and phenolics in leaves of angiosperms in response to eCO2 do not depend on temperature, responses to CO2 of other plant compounds such as non-structural carbohydrates, phenolics and
Nutritional quality and defenses
forest insect damage
Voltinism survival synergy
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Conceptual diagram showing the relationships between main components of climate change and the mechanisms explaining their effects on forest insect damage. The green arrows point the main effects of climate change drivers on forest insect performance and damage, that is, directly on insects’ survival and voltinism or indirectly through change of host tree abundance (breeding substrate), nutritional quality, and defenses. The red arrows illustrate some of the possible interactions between effects of climate change drivers: neutral (e.g. between drought and eCO2), negative (e.g. antagonistic effects of storm and drought on bark beetles, of temperature and eCO2 on nutritional quality of leaves for defoliators), or positive (e.g. synergistic effects of high temperature and storm on bark beetles, of temperature and drought on several forest insects). www.sciencedirect.com
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terpenes in woody tissues were seen only under elevated temperatures. Finally, climate change also affects interactions between herbivores and their natural enemies (reviewed by Ref. ). It is likely that responses of predators and parasitoids to combinations of climatic drivers will also differ from those to individual drivers as experimentally shown by Ref. .
Conclusions A few generalities emerge from the review of recent publications on the effects of climate change on forest insect pests. First, climate change is a multifaceted issue, with increased CO2 and other greenhouse gases triggering temperature and drought increase, which both can modify storm regime (Figure 1). All of these components can independently and interactively affect forest pest dynamics and behaviour (Figure 1). The main identified mechanisms of positive forest insect responses (i.e. more damage) to climate change are (i) higher number of generations per year and higher survival under warmer temperatures, (ii) lower tree resistance to insect attack under more severe droughts, (iii) higher amount of breeding substrate for bark beetles following storms, and (iv) changes in substrate quality for defoliators due to elevated CO2 (Figure 1). Although most of these effects are likely to result in increased forest damage, many particular but overlooked climate driven processes can have negative effects on insect herbivores in forests. For example, heat waves can increase insect mortality while moderate droughts can enhance induced defences. However, as emphasized in this review, climate change drivers are likely to interact (Figure 1) through either antagonistic relationships resulting in annihilation process (e.g. combined effects of eCO2 and higher temperatures on leaf quality for defoliators, and combined effects of storms and drought on breeding substrate for bark beetles) or positive relationships resulting in synergistic effects (e.g. hotter droughts benefiting defoliators, warmers storms benefiting bark beetles). In addition, most of the expected effects of climate change on herbivorous insects should also apply to insect predators or parasitoids. Recent studies have also shown that insect — tree interactions are mediated by mycorrhizal and endophytic fungi [59,60] or bacteria. How those microorganisms respond to climate change and whether their responses affect host tree resistance to insect herbivores are still open questions. Predicting the overall effects of climate change on interactions between trees, insect herbivores and associated organisms (antagonists or symbionts) and the resulting forest conditions thus remains particularly difficult, especially because these effects may scale non-linearly. This calls for in depth, holistic research on key biological models, where empirical data on species interactions under various climatic conditions would feed process-based models (e.g. ). Current Opinion in Insect Science 2019, 35:103–108
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment The French National Research Agency for the funding of the study under the research project DiPTiCC (ANR-16-CE32-0003).
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