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Insect herbivores are among the most abundant and diverse groups of animals in terrestrial ecosystems, and engage in complex interactions with their natural enemies, host plants, and microbial partners. I develop an experimental community ecology program to study these interactions, and to understand the ecological processes that shape plant-based terrestrial ecosystems. I study these interactions to provide fundamental ecological knowledge, but also to help manage species that have a negative impact on agricultural or forest ecosystems.

From 2019 I am a researcher at CBGP - Centre for Biology and Management of Populations - in Montpellier (France). This centre hosts personnel from different research institutions, and I belong to CIRAD - Agricultural Research for Development. Before I spent 3 years in Reunion island (France) as a CIRAD researcher studying the ecology of thrips and predatory mites. Most of my research as a postdoc at the University of Oxford (England) and at Wageningen University (the Netherlands) involved the study of indirect effects in aphid communities. My doctoral research at the Universitat de València (Spain) focused on the population ecology and life history evolution of the browntail moth Euproctis chrysorrhoea.

My main interests are:

- Insect population biology: plant effects and interactions with parasitoids.

- Indirect effects: apparent competition and plant-mediated interactions in insect communities.

- Insect symbionts and their consequences at the community level.

Access my publications via ResearchGate.

Looking for a MSc internship or thesis? Please contact me!

My main current project ENEMYCOCKTAIL funded by the French National Research Agency (ANR-PRCE).

Some of my publications

Many animals have evolved associations with symbiotic microbes that benefit the host through increased growth, lifespan, and survival. Some interactions are obligate (essential for survival) while others are facultative (usually beneficial but not essential). Not all individuals host all facultative symbionts in a population, and thus there is probably a trade-­off between the cost of hosting these symbionts and the benefits they confer to the host. Plant-­sucking insects have been one of the most important models to test these costs and benefits experimentally. This research is now moving beyond the description of symbiont effects towards understanding the mechanisms of action, and their role in the wider ecological community. We present a quantitative and systematic analysis of the published evidence exploring this question. We found that whitefly and true bugs experience benefits through increased growth and fecundity, whereas aphids experience costs to their fecundity but benefits through increased resistance to natural enemies. We also report the lack of data in some plant-sucking groups, and explore variation in effect strengths and directions across aphid host, symbiont and plant species thus highlighting the importance of considering the context dependency of these interactions.

R Kehoe, E Frago, D Sanders (2021) Cascading extinctions as a hidden driver of insect decline. Ecological Entomology (Review). Text.

In this review, we bring together theory and knowledge about secondary extinctions in the light of the main drivers of insect decline. We evaluate potential and evidence for cascading extinction for the different drivers and identify major pathways. By providing selected examples we discuss how habitat loss, pollution, species invasions, climate change and overexploitation can cause cascading extinctions. We argue that habitat loss and pollution in particular have the largest potential for such extinctions by changing community structure, the physical environment, and community robustness. 

Secondary extinctions (left figure) (a) Co-extinctions after the initial loss of a resource, (b) network transmitted extinctions driven by changes in interaction strength and indirect interactions. Red nodes (with an x) in the food web are going initially extinct with the orange nodes as secondary extinctions. The arrows indicate the transmission of the initial impact.

Drivers and cascading extinctions (right figure). Arrows with continuous lines depict direct interactions. Indirect effects of drivers on insect extinctions are also shown as dashed lines. The initial impact through drivers is shown by a red circle. Higher-trophic levels suffer from habitat loss as bottom-up effects are magnified along food chains (a1). Habitat degradation can increase the density of insect natural enemies and trigger insect extinctions (a2). Highly fertilized agricultural habitats increase pest densities with negative indirect effect on other insects through apparent competition (a3). The impact of habitat loss depends on insect functional traits including dispersal capabilities, longevity and specialisation (a4). Pollution in the form of herbicides and insecticides bioaccumulates along food chains (b1). These products can kill non-target organisms and trigger declines of pollinating insects thus altering plant-pollinator networks and plant communities (b2). Anthelmintic substances used to treat worm infestation in livestock alter dung beetle communities (b3). Since some of these beetles are plant pollinators, this can also alter plant-pollinator networks (b2). (c) Invasive species can trigger extinctions of local insects indirectly through shared natural enemies (i.e. apparent competition, c1), or by altering local plant communities and trigger bottom-up extinction cascades (c3). Invasive predators can become top-predators via intraguild predation and release certain populations of prey from top-down pressure thus increasing pressure on others (c2). (d) Climate change alters the synchrony between plants and herbivores. Some omnivorous herbivores (here mice) also predate on insects thus controlling their populations. This equilibrium can be altered, and pest outbreaks triggered with negative effects on non-pest species via resource competition (d1). Some insects rely on mutualistic symbioses (represented here as a red bacterium) to obtain protection from natural enemies. These symbionts are often susceptible to increased temperatures so that global warming can render these insects unprotected and susceptible to demise due to top-down pressure (d2).

Microbes play crucial roles in the biology of herbivorous insects, and the last decade has provided exciting new evidence for a prominent role of microbial symbiosis in detoxification of plant toxins, manipulation of plant defences and defence against natural enemies. We provide an order by order update of symbioses across herbivorous insects, particularly focusing on recent published evidence, and on how symbionts interact with the defensive system of the plant. While the hemimetabolous Hemiptera order largely relies on obligatory microbial symbioses, we did not find such a close relationship between symbionts and hosts in the other three orders Orthoptera, Phasmatodea and Thysanoptera. These three orders mostly harbour transient gut symbionts and/or rely on laterally transferred genes from microbes. Despite the radical changes and harsh conditions during metamorphosis, numerous holometabolous species transmit symbionts vertically and show close associations with both intra- and extracellular symbionts. The last section of this book chapter discusses the role that symbionts will play in future scenarios of global warming, but also their implications for the transmission of plant viruses and modern agriculture.

Although parasitoid competition has been debated and studied over the past several decades, understanding the factors that allow for coexistence among species sharing the same host in the field remains elusive. Parasitoids may be able to coexist on the same host species if they partition host resources according to size, age, or stage, or if their dynamics vary at spatial and temporal scales. One area that has thus far received little experimental attention is if competition can alter host usage strategies in parasitoids. In this study, we tested this hypothesis with two parasitoid species in the genus Aphytis, both of which are specialized on the citrus pest California red scale, Aonidiella aurantii. These parasitoids prefer large scales as hosts and yet coexist in sympatry in eastern parts of Spain. Parasitoids and hosts were sampled in 12 replicated orange groves. When host exploitation by the stronger competitor, A. melinus, was high the poorer competitor, A. chrysomphali, changed its foraging strategy to prefer alternative plant substrates where it parasitized hosts of smaller size. Consequently, the inferior parasitoid species shifted both its habitat and host size as a result of competition. Our results suggest that density-­dependent size-­mediated asymmetric competition is the likely mechanism allowing for the coexistence of these two species, and that the use of suboptimal (small) hosts can be advantageous under conditions imposed by competition where survival in higher quality larger hosts may be greatly reduced. Photo credit: Alejandro Tena

Parasitoids often engage in antagonistic interactions with higher order natural enemies like (a) intraguild predators and (b) hyperparasitoids. Direct trophic effects involve a consumer-resource interaction (black solid lines), whereas direct trait-mediated effects involve changes in the behaviour or morphology of the interacting species (yellow solid lines). Interactions among species can be indirect if they are mediated by at least a third species (yellow dashed lines). Herbivory has a direct effect on plant traits or defensive state (solid green lines), and also an indirect effect on parasitoid foraging through herbivore-induced plant volatiles (grey vapour lines). (a) Intraguild predators (represented by a ladybird) can reduce herbivore suppression by parasitoids by preying on parasitoid larvae (A1). Herbivore suppression, however, is influenced by the functional niche of the intraguild predator, and by the diversity of the community of natural enemies, at both the species and the phylogenetic level. Parasitoids detect and avoid chemical cues from intraguild predators (A2), and these responses can have consequences for host-parasitoid dynamics (A3). Risk of intraguild predation can alter parasitoid attraction to herbivore-induced plant volatiles (A4). Risk of predation can also affect the way herbivores feed on plants and hence plant volatile induction, with consequences for parasitoid foraging (A5). (b) Hyperparasitoids (top trophic level) attack primary parasitoids and can affect herbivore-parasitoid dynamics (B1). This effect, however, depends on the trophic web of herbivores, primary parasitoids and hyperparasitoids, and on the traits and evolutionary history of the species involved. Primary parasitoids detect and avoid chemical cues from hyperparasitoids (B2). Herbivory can affect plant traits or defensive state, and these changes can cascade up to the hyperparasitoid level (B3). Hyperparasitoids can use herbivore-induced plant volatiles to locate their hosts (B4). For both intraguild predation and hyperparasitism, these interactions are influenced by spatial complexity, at both the plant and the landscape level.

E. Frago & É. Bauce (2014) Life-history consequences of chronic nutritional stress in an outbreaking insect defoliator. PLoS ONE. In this study we  explored long term consequences of nutritional stress in the outbreaking moth Choristoneura fumiferana, one of the most economically important forest insect pest in north-eastern North America. We assessed the effect of offspring and parental diet on moth life history traits with generalised animal models fitted with Bayesian Markov chain Monte Carlo (MCMC) techniques. We found no evidence of nutritional stress in the parental generation increasing offspring ability to feed on low quality diet, but the contrary: compared to offspring from parents that were fed a high quality diet (grey bars), larvae from parents fed a low quality diet (white bars) had increased mortality, reduced growth rate and reduced female reproductive output. Density-dependent deterioration in plant quality is thought to be an important factor governing the population dynamics of outbreaking insects and we hypothesise that chronic nutritional stress can be a driver of outbreak declines of C. fumiferana, and of forest insects in general.

E. Frago, M. Dicke & H.C.J. Godfray (2012) Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology & Evolution. Abstract.

Pictures. Left: field study on plant-mediated indirect effects between pea aphids, Acyrthosiphon pisum, and grain aphids, Sitobion avenae. Right: third instar browntail moth, Euproctis chrysorrhoea, larvae feeding on fresh leaves of the strawberry tree, Arbutus unedo.