Impacts of climate change on the performance of an insect pest and associated consequences for tritrophic interactions

Le réchauffement climatique va avoir des répercussions profondes sur les organismes vivants, en particulier les ectothermes comme les insectes, dont la physiologie et le comportement sont intimement liés à la température de leur environnement. Cette thèse propose d’étudier, par voie expérimentale, les conséquences du réchauffement climatique sur la performance d’un ravageur majeur de la vigne en Europe, l’eudémis (Lobesia botrana), et les conséquences pour l’interaction entre ce phytophage et les niveaux trophiques associés, en particulier les ennemis naturels (parasitoïdes). Les travaux se focalisent sur trois facettes du réchauffement climatique : une augmentation de température moyenne, une altération de l’amplitude thermique journalière, et l’occurrence d’une vague de chaleur.Les résultats attestent d’un impact des températures sur les traits reliés à la performance larvaire (capacités de défense des chenilles contre les ennemis naturels) et sur la reproduction des adultes, ainsi que sur l’interaction entre ce ravageur et un parasitoïde oophage. Par ailleurs, une importante variabilité de réponses thermiques est observée entre traits et parfois entre facettes du changement climatique, laissant suggérer des conséquences complexes de ce dernier sur la dynamique des populations du ravageur. Ainsi, prédire la réponse d’une espèce au réchauffement climatique nécessite d’adopter une vision relativement intégrative de la biologie de cette espèce, ainsi que de la complexité des changements se produisant au niveau de l’environnement thermique de l’organisme.Global warming poses a major challenge to living organisms, particularly for ectothermic animals like insects, whose physiology and behaviour are closely related with direct thermal surroundings. This thesis aims at experimentally investigating the impacts of climate change on the overall performance of a major grapevine pest, the European grapevine moth (Lobesia botrana), and the associated consequences for interactions involving this phytophagous insect and adjacent trophic levels, more specifically natural enemies (parasitoids). The experiments conducted focus on three facets of climate change: an increase in mean temperature, an alteration of daily thermal range, and the occurrence of heat waves as extreme thermal events.Results highlight an impact of temperatures on both life-history traits related with larval performance (defensive abilities of caterpillars) and adult reproductive success, with demonstrated repercussions for the interaction between this pest and an oophagous parasitoid. Furthermore, they reveal an important variability of thermal responses occurring among traits and even facets of climate change, thereby suggesting complex consequences of this phenomenon in terms of pest population dynamics. Hence, predicting a species response to climate change requires adopting an integrative perspective of the biology of the focal species while considering the complexity of changes occurring in insect direct thermal environment

Effets du réchauffement climatique sur la performance d’un ravageur des cultures et impact sur les relations tritrophiques

Global warming poses a major challenge to living organisms, particularly for ectothermic animals like insects, whose physiology and behaviour are closely related with direct thermal surroundings. This thesis aims at experimentally investigating the impacts of climate change on the overall performance of a major grapevine pest, the European grapevine moth (Lobesia botrana), and the associated consequences for interactions involving this phytophagous insect and adjacent trophic levels, more specifically natural enemies (parasitoids). The experiments conducted focus on three facets of climate change: an increase in mean temperature, an alteration of daily thermal range, and the occurrence of heat waves as extreme thermal events.Results highlight an impact of temperatures on both life-history traits related with larval performance (defensive abilities of caterpillars) and adult reproductive success, with demonstrated repercussions for the interaction between this pest and an oophagous parasitoid. Furthermore, they reveal an important variability of thermal responses occurring among traits and even facets of climate change, thereby suggesting complex consequences of this phenomenon in terms of pest population dynamics. Hence, predicting a species response to climate change requires adopting an integrative perspective of the biology of the focal species while considering the complexity of changes occurring in insect direct thermal environment.Le réchauffement climatique va avoir des répercussions profondes sur les organismes vivants, en particulier les ectothermes comme les insectes, dont la physiologie et le comportement sont intimement liés à la température de leur environnement. Cette thèse propose d’étudier, par voie expérimentale, les conséquences du réchauffement climatique sur la performance d’un ravageur majeur de la vigne en Europe, l’eudémis (Lobesia botrana), et les conséquences pour l’interaction entre ce phytophage et les niveaux trophiques associés, en particulier les ennemis naturels (parasitoïdes). Les travaux se focalisent sur trois facettes du réchauffement climatique : une augmentation de température moyenne, une altération de l’amplitude thermique journalière, et l’occurrence d’une vague de chaleur.Les résultats attestent d’un impact des températures sur les traits reliés à la performance larvaire (capacités de défense des chenilles contre les ennemis naturels) et sur la reproduction des adultes, ainsi que sur l’interaction entre ce ravageur et un parasitoïde oophage. Par ailleurs, une importante variabilité de réponses thermiques est observée entre traits et parfois entre facettes du changement climatique, laissant suggérer des conséquences complexes de ce dernier sur la dynamique des populations du ravageur. Ainsi, prédire la réponse d’une espèce au réchauffement climatique nécessite d’adopter une vision relativement intégrative de la biologie de cette espèce, ainsi que de la complexité des changements se produisant au niveau de l’environnement thermique de l’organisme

Impact of heat stress on the fitness outcomes of symbiotic infection in aphids: a meta-analysis

International audienceBeneficial microorganisms shape the evolutionary trajectories of their hosts, facilitating or constraining the colonization of new ecological niches. One convincing example entails the responses of insect-microbe associations to rising temperatures. Indeed, insect resilience to stressful high temperatures depends on the genetic identity of the obligate symbiont and the presence of heat-protective facultative symbionts. As extensively studied organisms, aphids and their endosymbiotic bacteria represent valuable models to address eco-evolutionary questions about the thermal ecology of insect-microbe partnerships, with broad relevance to various biological systems and insect models. This meta-analysis aims to quantify the context-dependent impacts of symbionts on host phenotype in benign or stressful heat conditions, across fitness traits, types of heat stress and symbiont species. We found that warming lowered the benefits (resistance to parasitoids) and costs (development, fecundity) of infection by facultative symbionts, which was overall mostly beneficial to the hosts under short-term heat stress (heat shock) rather than extended warming. Heat-tolerant genotypes of the obligate symbiont Buchnera aphidicola and some facultative symbionts (Rickettsia sp., Serratia symbiotica) improved or maintained aphid fitness under heat stress. We discuss the implications of these findings for the general understanding of the cost-benefit balance of insect-microbe associations across multiple traits and their eco-evolutionary dynamics faced with climate change

Where you come from matters: temperature influences host-parasitoid interaction through parental effects.

11 pagesInternational audienceTemperature alters host suitability for parasitoid development through direct and indirect pathways. Direct effects depend on ambient temperatures experienced by a single host individual during its lifetime. Indirect effects (or parental effects) occur when thermal conditions met by a host parental generation affect the way its offspring will interact with parasitoids. Using the complex involving eggs of the moth Lobesia botrana as hosts for the parasitoid Trichogramma cacoeciae, we developed an experimental design to disentangle the effects of (1) host parental temperature (temperature at which the host parental generation developed and laid host eggs) and (2) host offspring temperature (temperature at which host eggs were incubated following parasitism, i.e. direct thermal effects) on this interaction. The host parental generation was impacted by temperature experienced during its development: L. botrana females exposed to warmer conditions displayed a lower pupal mass but laid more host eggs over a 12-h period. Host parental temperature also affected the outcomes of the interaction. Trichogramma cacoeciae exhibited lower emergence rates but higher hind tibia length on emergence from eggs laid under warm conditions, even if they were themselves exposed to cooler temperatures. Such indirect thermal effects might arise from a low nutritional quality and/or a high immunity of host eggs laid in warm conditions. By contrast with host parental temperature, offspring temperature (direct thermal effects) did not significantly affect the outcomes of the interaction. This work emphasises the importance of accounting for parental thermal effects to predict the future of trophic dynamics under global warming scenarios

Parasitism may alter functional response comparisons: a case study on the killer shrimp Dikerogammarus villosus and two non-invasive gammarids

The Ponto-Caspian freshwater amphipod Dikerogammarus villosus has colonized most of the water bodies of continental Europe where it causes strong structural alterations in recipient communities that can lead to changes in ecosystem-level processes, mainly because of a strong predatory behaviour. Most of the D. villosus populations from the invaded range have been found infected with the co-introduced microsporidian parasite Cucumispora dikerogammari, known to decrease the predation rate of its host. Infection might thus mitigate the ecological impact of D. villosus and we wanted to test this assumption using the comparative functional response approach. We compared the relationship between resource use and resource availability (i.e. the functional response, FR) of D. villosus, either with infected individuals or not, to that of two non-invasive gammarids: Gammarus pulex and Echinogammarus berilloni. With infected individuals included, D. villosus displayed a higher FR than the two non-invasive gammarids. Although this effect was not significant, C. dikerogammari infection tended to alter the FR of D. villosus with a slight decrease in attack rate and handling time, resulting in a less steep initial slope and a higher asymptote, respectively. Removing infected D. villosus from the dataset did not affect the FR comparison with G. pulex but suppressed the difference in FR with E. berilloni. Although we cannot exclude the role of sample size reduction in this effect, this suggests that C. dikerogammari infection might increase the predation pressure on local prey populations in case of species replacement between D. villosus and E. berilloni. From a more general perspective, our study illustrates how parasites may alter our capacity to predict invasive species impacts from FR comparisons

A perspective on insect–microbe holobionts facing thermal fluctuations in a climate‐change context

Temperature influences the ecology and evolution of insects and their symbionts by impacting each partner independently and their interactions, considering the holobiont as a primary unit of selection. There are sound data about the responses of these partnerships to constant temperatures and sporadic thermal stress (mostly heat shock). However, the current understanding of the thermal ecology of insect–microbe holobionts remains patchy because the complex thermal fluctuations (at different spatial and temporal scales) experienced by these organisms in nature have often been overlooked experimentally. This may drastically constrain our ability to predict the fate of mutualistic interactions under climate change, which will alter both mean temperatures and thermal variability. Here, we tackle down these issues by focusing on the effects of temperature fluctuations on the evolutionary ecology of insect–microbe holobionts. We propose potentially worth-investigating research avenues to (i) evaluate the relevance of theoretical concepts used to predict the biological impacts of temperature fluctuations when applied to holobionts; (ii) acknowledge the plastic (behavioural thermoregulation, physiological acclimation) and genetic responses (evolution) expressed by holobionts in fluctuating thermal environments; and (iii) explore the potential impacts of previously unconsidered patterns of temperature fluctuations on the outcomes and the dynamic of these insect–microbe associations

Reproductive performance of the European grapevine moth Lobesia botrana (Tortricidae) is adversely affected by warming scenario

The European grapevine moth, Lobesia botrana (Denis and Schiffermüller), is an important grape pest worldwide. To forecast how this species might respond to climate change has emerged as one major challenge in recent viticultural research. Predictions about L. botrana population dynamics under global warming scenario are usually derived from physiologically based demographic models (PBDMs). Despite their ecological realism, PBDMs are based on physiological equations derived from constant, unrealistic thermal regimes, and they exclude the effects of temperature on male’s reproductive traits, which importantly mediates population dynamics in this species. Focused on Burgundy (a viticultural region of France), we compared the adult performance of L. botrana between the Current Fluctuating Regime (CFR) based on in situ meteorological data and the Future Fluctuating Regime (FFR) based on the outputs of climate models. Under controlled conditions complying to the scenario of local warming termed FFR, L. botrana individuals incurred reduced adult lifespan, while their body amounts of four major energetic components (proteins, lipids, glycogen, soluble carbohydrates) remained unchanged compared to individuals exposed to the CFR. Furthermore, each sex endured reproductive costs associated with local warming scenario: females incurred reduced mating success, and males bore decreased fertility (lower number of eupyrene sperms within spermatophore). Our results indicate that global warming should adversely impact the reproductive success of L. botrana and the local abundance of this pest. In terms of pest management, our findings might contribute to the increase in the ecological realism of PBDMs and improve the reliability of their predictions about the population dynamics of L. botrana

Warming increases tolerance of an insect pest to fungicide exposure through temperature-mediated hormesis

Pest management strategies relying on agrochemicals could be altered by climate change, because of the temperature-dependent toxicity of the compound involved. Many studies have explored the response of targeted pests to pesticide and temperature. Pesticides are seldom strictly selective and also affect nontarget pests. Surprisingly, the way temperature may shape these side effects of pesticides remains overlooked, limiting our understanding of the net impacts of future chemical treatments on the overall damage induced by different pests. We investigated how temperature modulates the response of a major grape insect pest (the tortricid moth Lobesia botrana) to a copper-based fungicide. We examined the lethal (larval survival) and sublethal (larval development, pupal mass, immune parameters) effects of exposure to different concentrations of copper in larval food. We found that copper concentration had negative linear effects on larval development and pupal mass. In addition, copper concentration had biphasic curvilinear effects on total phenoloxidase activity, which is indicative of hormesis (stimulation and inhibition of insect performance at low and high copper concentrations, respectively). Temperature stimulated development, while compromising immunity (total phenoloxidase activity). Significant interaction between copper concentration and temperature was detected for larval survival and phenoloxidase activity: warmer conditions improved pest tolerance to copper through temperature-driven hormesis (larval survival) or by shifting the hormesis-related peak of performance toward higher copper concentrations (phenoloxidase activity). This combination of simple and interactive effects could propagate to populations, communities and agroecosystem, with implications for future management of viticultural pests

When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest.

12 pagesInternational audiencePhytophagous insects evolving in agroecosystems express numerous defences when faced with myriads of natural enemies. Such defensive traits might impair the effectiveness of biological control relying on these natural enemies, mostly parasitoids. In the case of parasitoid threat, these defences consist of the avoidance of the parasitoid (reduced exposure to antagonists through shortening of developmental time), hindrance of oviposition (evasive behaviours and morphological protection) or destruction of the parasitoid eggs (encapsulation and melanisation by means of the immune system). Previous works focused on one defensive trait only when investigating the effects of temperature on host resistance. By doing so, they assumed that all defensive traits would respond uniformly to a change occurring in thermal environment, which remains an undocumented fact. To test this assumption in the context of global warming, we adopted a global overview of host resistance by examining the effects of rising temperatures on multiple defensive traits used by the grape pest, Lobesia botrana, against its larval parasitoids. Although warmer conditions led to reduced exposure to parasitoids by accelerating larval development, warmer conditions also elicited extensive weakening of behavioural and immune defences. These results confirm that temperatures might differently modulate the levels of expression of several defensive traits. An increase in growth rate and pupal mass also occurred, especially for females, which may contribute to greater pest fecundity in the future. However, the decline of L. botrana resistance might enhance the efficiency of the biological control naturally exerted by parasitoids in vineyards, thereby limiting the damage to crops