Adverse effects of the Bordeaux mixture copper-based fungicide on the non-target vineyard pest Lobesia botrana.

BACKGROUND: Bordeaux mixture is a copper-based fungicide commonly used in vineyards to prevent fungal and bacterial infections in grapevines. However, this fungicide may adversely affect the entomological component, including insect pests. Understanding the impacts of Bordeaux mixture on the vineyard pest Lobesia botrana is an increasing concern in the viticultural production. RESULTS: Bordeaux mixture had detrimental effects on the development and reproductive performance of L. botrana. Several physiological traits were adversely affected by copper-based fungicide exposure, including a decrease in larval survival and a delayed larval development to moth emergence, as well as a reduced reproductive performance through a decrease in female fecundity and fertility and male sperm quality. However, we did not detect any effect of Bordeaux mixture on the measured reproductive behaviors (mating success, pre-mating latency and mating duration). CONCLUSION: Ingestion by larvae of food contaminated with Bordeaux mixture had a negative effect on the reproductive performance of the pest L. botrana, which could affect its population dynamics in vineyards. Although this study highlighted collateral damage of Bordeaux mixture on L. botrana, the potential impact of copper-based fungicides on vineyard diversity, including natural predators is discussed and needs to be taken in consideration in integrated pest management. © 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Consistent variations in personality traits and their potential for genetic improvement in biocontrol agents: Trichogramma evanescens as a case study.

Improvements in the biological control of agricultural pests require improvements in the phenotyping methods used by practitioners to select efficient biological control agent (BCA) populations in industrial rearing or field conditions. Consistent inter-individual variations in behaviour (i.e. animal personality) probably affect BCA efficiency, but have never been taken into account in the development of phenotyping methods, despite having characteristics useful for phenotyping: repeatable (by definition), often heritable, etc. We developed a video-tracking method targeting animal personality traits and evaluated the feasibility of its use for genetic improvement in the BCA Trichogramma evanescens, by phenotyping 1,049 individuals from 24 isogenic lines. We found consistent individual variations in boldness, activity and exploration. Personality differences between the 24 isogenic lines suggested a genetic origin of the variations in activity and exploration (broad-sense heritability estimates of 0.06 to 0.11) and revealed a trade-off between exploration and fecundity.

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.

Sexual audience affects male's reproduction investment without consequences on reproductive outputs.

Males evolved plastic strategies to respond to male-male competition and exhibit adaptive traits and behaviors maximizing their access to the females and limiting sperm competition. Mating behaviors allow males to express quick responses to current sexual audience, that is, the number of nearby conspecifics prone to mate. In contrast, physiological responses are frequently delayed because they are constrained by the time and resources having to be mobilized to produce and export sperm and associated products. This is especially critical in species for which males produce spermatophores. Here we investigated in what extend moth males (the tortricid moth Lobesia botrana) producing spermatophores exhibit plastic behavioral and physiological responses to different sexual audiences before and during mating and the consequences for their reproductive output. We found that males adjusted their mating behaviors and spermatophore size to a potentially elevated risk of sperm competition perceived before mating. In addition, males responded to the closed presence of females during mating by reducing their mating duration. Surprisingly, the various behavioral and physiological responses we highlighted here were not fully reflected in their reproductive performance as we did not reveal any effect on fecundity and fertility of their mate. The selective pressure exerted on males experiencing male-male competition could thus be sufficient to trigger adjustment in male mating behaviors but constrains physiological responses according to the perception of competition.

How to stand the heat? Post-stress nutrition and developmental stage determine insect response to a heat wave.

Organisms are increasingly confronted with intense and long-lasting heat waves. In insects, the effects of heat waves on individual performance can vary in magnitude both within (e.g. from one larval instar to another) and between life stages. However, the reasons underlying these stage-dependent effects are not fully understood. There are several lines of evidence suggesting that individual ability to withstand a heat stress depends on mechanisms based on nutrition and supporting energetically physiological stress responses. Hence, we tested the hypothesis that the efficiency of these food-based buffering mechanisms may vary between different larval instars of a phytophagous insect. Using larvae of the moth Lobesia botrana, we examined the importance of post-stress food quality in insect response to a non-lethal heat wave at two distinct larval instars. Three major conclusions were drawn from this work. First, heat waves induced an overall decline in larval performance (delayed development, depressed immunity). Second, food quality primarily mediated the insect's ability to respond to the heat stress: the reduction in performance following heat wave application was mostly restricted to individuals with access to low-quality food after the heat stress. Third, larval instars differed in their susceptibility to this combination of thermal and food stressors, but conclusions about the instar being the most vulnerable differed in a trait-specific manner. In a global warming context, this study may shed additional light on the combination of direct and indirect (through alteration of plant nutritional value) effects of rising temperatures on the ecology and the evolution of phytophagous insects.

Measuring the evolutionary potential of a winter-active parasitic wasp to climate change.

In temperate climates, as a consequence of warming winters, an increasing number of ectothermic species are remaining active throughout winter months instead of diapausing, rendering them increasingly vulnerable to unpredictable cold events. One species displaying a shift in overwintering strategy is the parasitoid wasp and biological control agent Aphidius avenae. The current study aimed to better understand the consequence of a changing overwintering strategy on the evolutionary potential of an insect population to adapt to the cold stress events, set to increase in frequency, even during milder winters. Using a parental half-sibling breeding design, narrow-sense heritability of the cold tolerance, morphology and longevity of A. avenae was estimated. The heritability of cold tolerance was estimated at 0.07 (CI95% = [0.00; 0.25]) for the Critical Thermal Minima (CTmin) and 0.11 (CI95% = [0.00; 0.34]) for chill coma temperature; estimates much lower than those obtained for morphological traits (tibia length 0.20 (CI95% = [0.03; 0.37]); head width 0.23 (CI95% = [0.09; 0.39]); wing surface area 0.28 (CI95% = [0.11; 0.47])), although comparable with the heritability estimate of 0.12 obtained for longevity (CI95% = [0.00; 0.25]). The heritability estimates obtained thus suggest that A. avenae possesses low adaptive potential against cold stress. If such estimates are indicative of the evolutionary potential of A. avenae cold tolerance, more emphasis may be placed on adaptive phenotypic plasticity at the individual level to persist in a changing climate, with potential implications for the biological control function they provide.

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

Temperature 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.

Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling.

Predicting species responses to climate change requires tracking the variation in individual performance following exposure to warming conditions. One ecologically relevant approach consists of examining the thermal responses of a large number of traits, both related with population dynamics and trophic interactions (i.e. a multi-trait approach). Based on in situ climatic data and projections from climate models, we here designed two daily fluctuating thermal regimes realistically reflecting current and future conditions in Eastern France. These models detected an increase in mean temperature and in the range of daily thermal fluctuations as two local facets of global warming likely to occur in our study area by the end of this century. We then examined the responses of several fitness-related traits in caterpillars of the moth Lobesia botrana - including development, pupal mass, survival rates, energetic reserves, behavioral and immune traits expressed against parasitoids - to this experimental imitation of global warming. Increasing temperatures positively affected development (leading to a 31% reduction in the time needed to complete larval stage), survival rates (+19%), and movement speed as a surrogate for larval escape ability to natural enemies (+60%). Conversely, warming elicited detrimental effects on lipid reserves (-26%) and immunity (total phenoloxidase activity: -34%). These findings confirm that traits should differ in their sensitivity to global warming, underlying complex consequences for population dynamics and trophic interactions. Our study strengthens the importance of combining a multi-trait approach with the use of realistic fluctuating regimes to forecast the consequences of global warming for individuals, species and species assemblages.

Pair-bonding influences affective state in a monogamous fish species.

In humans, affective states are a key component in pair-bonding, particularly in the early stage of a relationship. Pairing with a high-quality partner elicits positive affective states which, in turn, validate and reinforce the mate choice. Affective states thus strongly affect pair stability and future reproductive success. We propose generalizing the link between affective states and pair-bonding to encompass other monogamous species exhibiting biparental care, chiefly where the reproductive success of the pair critically depends on the coordination between partners. The convict cichlid Amatitlania siquia is a monogamous fish species that forms long-lasting pairs with strong cooperation between parents for parental care. In this species, we showed that females paired with their non-preferred male had lower reproductive success than those paired with their preferred male. We then transposed the judgement bias paradigm, previously used in other animal species, to assess objectively affective states in fishes. Females that were assigned their non-preferred partner exhibited pessimistic bias, which indicates a negative affective state. By contrast, females that were assigned their preferred partner did not exhibit changes in their affective state. Our results highlight that the influence of pair-bonding on affective states is not human-specific and can also be observed in non-human species.

When parasitoids deal with the spatial distribution of their hosts: consequences for both partners.

Insect parasitoids developing inside hosts face a true challenge: hosts are scattered in the field and their localization and selection require the use of complex and sometime confusing information. It was assumed for a long time that small-brained organisms like parasitoids have evolved simple and efficient behavioral mechanisms, leading them to be adapted to a given ecological situation, for example, the spatial distribution of hosts in the habitat. However, hosts are not static and their distribution may also vary through generations and within the life of parasitoid individuals. We investigated if and how parasitoids deal with such a spatial complexity in a mesocosm experiment. We used the Aphidius rhopalosiphi/Sitobion avenae parasitoid/host system to investigate if parasitoid females experiencing different host aggregation levels exhibit different foraging behaviors independently of the number of hosts in the environment. We showed that A. rhopalosiphi females exploited hosts more intensively both within and among patches at higher host aggregation levels. We discussed the adaptiveness of such behaviors in the light of evolution and biological control.

Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms.

Patch time allocation has received much attention in the context of optimal foraging theory, including the effect of environmental variables. We investigated the direct role of temperature on patch time allocation by parasitoids through physiological and behavioural mechanisms and its indirect role via changes in sex allocation and behavioural defences of the hosts. We compared the influence of foraging temperature on patch residence time between an egg parasitoid, Trichogramma euproctidis, and an aphid parasitoid, Aphidius ervi. The latter attacks hosts that are able to actively defend themselves, and may thus indirectly influence patch time allocation of the parasitoid. Patch residence time decreased with an increase in temperature in both species. The increased activity levels with warming, as evidenced by the increase in walking speed, partially explained these variations, but other mechanisms were involved. In T. euproctidis, the ability to externally discriminate parasitised hosts decreased at low temperature, resulting in a longer patch residence time. Changes in sex allocation with temperature did not explain changes in patch time allocation in this species. For A. ervi, we observed that aphids frequently escaped at intermediate temperature and defended themselves aggressively at high temperature, but displayed few defence mechanisms at low temperature. These defensive behaviours resulted in a decreased patch residence time for the parasitoid and partly explained the fact that A. ervi remained for a shorter time at the intermediate and high temperatures than at the lowest temperature. Our results suggest that global warming may affect host-parasitoid interactions through complex mechanisms including both direct and indirect effects on parasitoid patch time allocation.

The male mate search: an optimal foraging issue?

Male insects must find and mate females to have some descendants; male fitness therefore depends on the number of females they inseminate. Males are for this reason expected to optimize the behaviors related to mate location, orientation and copulation. Although optimization of the reproductive behavior of males has long been neglected in the literature, recent studies suggest a renewed interest for this idea. Here we discuss the parallel between male mate-finding and mating strategies in insects and optimal foraging theory (OFT), a class of models which formalize the behavior of organisms seeking and exploiting resources, generally food. We highlight the different facets of male mating systems allowing such a parallel, and claim for a unifying approach of foraging behavior. Finally, we discuss novel research perspective emerging from the application of OFT to male reproductive behavior.

Sperm-depleted males influence the reproductive behaviour of conspecifics.

In many insect species, sperm-depleted males (SDMs, i.e. males that have exhausted their sperm after a given number of matings) remain sexually active and continue to mate females. Here, we investigated the behavioural modifications that occur in both sexes of the parasitoid Asobara tabida Nees (Hymenoptera: Braconidae), after matings by fertile males and sperm-depleted males. We show that (i) virgin females, mated females and females mated to a SDM exhibited different behaviours and that (ii) males responded differently to females depending on whether the females had previously mated with an SDM or not. Our findings demonstrate that SDM influenced the reproductive behaviour of both males and females, especially with regard to male responsiveness and female attractiveness. These findings are discussed in the context of adaptive behaviour and fitness maximization in both males and females.

When parasitoid males make decisions: information used when foraging for females.

Optimal foraging models predict how an organism allocates its time and energy while foraging for aggregated resources. These models have been successfully applied to organisms such as predators looking for prey, female parasitoids looking for hosts, or herbivorous searching for food. In this study, information use and patch time allocation were investigated using male parasitoids looking for mates. The influence of the former presence of females in absence of mates and the occurrence of mating and other reproductive behaviours on the patch leaving tendency was investigated for the larval parasitoid Asobara tabida. Although males do not modify their patch residence time based on the number of females that visited the patch, they do show an increase in the patch residence time after mating a virgin female and performing courtship behaviour such as opening their wings. These results are in concordance with an incremental mechanism, as it has been described for females of the same species while foraging for hosts. The similarities between males and females of the same species, and the conditions under which such a patch-leaving decision rule is fitted are discussed. This is the first study describing an incremental effect of mating on patch residence time in males, thus suggesting that similar information use are probably driving different organisms foraging for resource, regardless of its nature.

Carbon dioxide narcosis modifies the patch leaving decision of foraging parasitoids.

Gleaning information is a way for foragers to adjust their behavior in order to maximize their fitness. Information decreases the uncertainty about the environment and could help foragers to accurately estimate environmental characteristics. In a patchy resource, information sampled during previous patch visits is efficient only if it is retained in the memory and retrieved upon arrival in a new patch. In this study, we tested whether the braconid Asobara tabida, a parasitoid of Drosophila larvae, retains information gleaned on patch quality in the memory and adjusts its foraging behavior accordingly. Females were anesthetized with CO(2) after leaving a first patch containing a different number of hosts and were allowed to visit a second patch containing only kairomones. CO(2) is known to erase unconsolidated information from the memory. We show that in the absence of a short CO(2) narcosis, females responded according to their previous experience, whereas anesthetized females did not. The anesthetized females stayed a given time in the second patch irrespective of what they encountered before. CO(2) narcosis had no effect on the residence time of the non-experienced females in a patch containing hosts or only kairomones in comparison with the non-anesthetized females that had a previous foraging experience. We conclude that CO(2) narcosis erases the effect of the previous patch quality, perhaps due to a memory disruption. Direct information processing is likely to be involved in parasitoid decision making through retention of the information on the previous patch quality into a CO(2) sensitive memory.

Humans and insects decide in similar ways.

Behavioral ecologists assume that animals use a motivational mechanism for decisions such as action selection and time allocation, allowing the maximization of their fitness. They consider both the proximate and ultimate causes of behavior in order to understand this type of decision-making in animals. Experimental psychologists and neuroeconomists also study how agents make decisions but they consider the proximate causes of the behavior. In the case of patch-leaving, motivation-based decision-making remains simple speculation. In contrast to other animals, human beings can assess and evaluate their own motivation by an introspection process. It is then possible to study the declared motivation of humans during decision-making and discuss the mechanism used as well as its evolutionary significance. In this study, we combine both the proximate and ultimate causes of behavior for a better understanding of the human decision-making process. We show for the first time ever that human subjects use a motivational mechanism similar to small insects such as parasitoids and bumblebees to decide when to leave a patch. This result is relevant for behavioral ecologists as it supports the biological realism of this mechanism. Humans seem to use a motivational mechanism of decision making known to be adaptive to a heterogeneously distributed resource. As hypothesized by Hutchinson et al. and Wilke and Todd, our results are consistent with the evolutionary shaping of decision making because hominoids were hunters and gatherers on food patches for more than two million years. We discuss the plausibility of a neural basis for the motivation mechanism highlighted here, bridging the gap between behavioral ecology and neuroeconomy. Thus, both the motivational mechanism observed here and the neuroeconomy findings are most likely adaptations that were selected for during ancestral times.