Enric Frago

Researcher at CIRAD - Agricultural Research for Development
UMR PVBMT - Unité Mixte de Recherche: Peuplements Végétaux et Bioagresseurs en Milieu Tropical
Saint-Pierre, La Réunion, France

enric.frago -at- cirad.fr
tel +262(0)693417586 / +262(0)262492740
Follow me on Twitter @EnricFrago


Insects are one of the most abundant and diverse group of animals on Earth, and I study them to understand the ecological processes that shape plant-based terrestrial ecosystems. Insect herbivores engage in complex interactions with their natural enemies, their host plants, and with microbial partners associated with these three trophic levels. Understanding these interactions will provide fundamental ecological knowledge, but it can also help manage species that have a negative impact on agricultural or forest ecosystems.

Currently I work as a researcher at CIRAD in Réunion island where I am studying the ecology of whiteflies and thrips. I am developing an experimental community ecology program to understand and control pest species in greenhouses. This program involves the study of indirect effects, a type of interaction that occurs when two members in a community (whether they are insects, plants or microbes) interact through a third player. In particular, I explore the role of natural enemies in mediating apparent competition and mutualism, plant-mediated indirect interactions, and the role of insect symbionts in this context.

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.

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

Recent Publications (2017)

E. Frago, M. Mala, B.T. Weldegergis, C. Yang, A. McLean, H.C.J. Godfray, R. Gols, M. Dicke (2017) Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles.  Nature Communications 8, 1860. Full text (Open access). Press release by Wageningen University.

Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores’ specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack. Here we demonstrate that the two phenomena can be linked. Plants fed upon by pea aphids release volatiles that attract parasitic wasps, and the pea aphid can carry facultative endosymbiotic bacteria that prevent the development of the parasitic wasp larva and thus markedly improve aphid survival after wasp attack. We show that these endosymbionts also attenuate the systemic release of volatiles by plants after aphid attack, reducing parasitic wasp recruitment and increasing aphid fitness. Our results reveal a novel mechanism through which symbionts can benefit their hosts and emphasise the importance of considering the microbiome in understanding insect ecological interactions.

N.H. Davila Olivas, E. Frago, M.P.M. Thoen, K.J. Kloth, F.F.M. Becker, J.J.A. van Loon, G. Gort, J.J.B. Keurentjes, J.van Heerwaarden, M. Dicke (2017) Natural variation in life‐history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds. Molecular Ecology 26: 2959–2977. Full text (Open access)

Recent Publications (2016)

D. Sanders, R. Kehoe, F.J.F. Van Veen, A. McLean, H.C.J. Godfray, M. Dicke, R. Gols, E. Frago (2016) Defensive insect symbiont leads to cascading extinctions and community collapse
. Ecology Letters,
19: 789–799. Full text.

In this study, we explore the effect of a defensive symbiont on population dynamics and species extinctions in an experimental community composed of three aphid species and their associated specialist parasitoids. We found that introducing a bacterial symbiont with a protective (but not a non-protective) phenotype into one aphid species led to it being able to escape from its natural enemy and increase in density. This changed the relative density of the three aphid species which resulted in the extinction of the two other parasitoid species. Our results show that defensive symbionts can cause extinction cascades in experimental communities and so may play a significant role in the stability of consumer-herbivore communities in the field.

A. Pekas, A. Tena, J.A. Harvey, F. Garcia-Marí & E. Frago (2016) Host size and spatiotemporal patterns mediate the coexistence of specialist parasitoids. Ecology, 97(5), 2016, pp. 1345–1356. Abstract.

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

E. Frago (2016) Interactions between parasitoids and higher order natural enemies: intraguild predation and hyperparasitoids. Current Opinion in Insect Science, 14:81–86. Abstract

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.

Older publications (2012-2015)

F.G. Pashalidou, E. Frago, E. Griese, E.H. Poelman, J.J.A. van Loon, M. Dicke & N.E. Fatouros (2015) Early herbivore alert matters: plant-mediated effects of egg deposition on higher trophic levels benefit plant fitness. Ecology Letters, 18(9): 927:936. Abstract.

Mustard plants are able to defend themselves against herbivores before these emerge from their eggs. Egg laying by female butterflies triggers a defensive response that has a negative impact on developing caterpillars, and parasitoids up to the fourth trophic level. Parasitism rates are also increased ultimately increasing plant reproductive output.

See press release by Wageningen University.

In the Figure a trophic web on Brassica nigra plants that was studied in the field can be seen. Primary parasitoids of the third trophic level attack the caterpillars (i.e. the gregarious endoparasitoid Cotesia glomerata) and pupae (i.e. the gregarious endoparasitoid Pteromalus puparum) of the large cabbage white butterfly Pieris brassicae of the second trophic level. The larvae of the primary parasitoid C. glomerata inside the herbivore host are attacked by the hyperparasitoid Baryscapus galactopus and C. glomerata cocoons are attacked by Lysibia nana, both wasps belonging to the fourth trophic level. The effects of the two different treatments were tested on the performance and the parasitisation rate of insects at the second, third and fourth trophic levels. EF plants were exposed to P. brassicae Egg deposition and subsequent larval Feeding (plant on the right) and F plants were exposed to larval Feeding only (plant on the left). Photo credits: www.bugsinthepicture.com.

J. Lazebnik, E. Frago, M. Dicke & J.J.A. van Loon (2014) Phytohormone mediation of interactions between herbivores and plant pathogens.

Journal of Chemical Ecology

In this review we present an overview of plant-mediated effects of plant pathogens on insect herbivores, and of insects on pathogens. Based on the phytohormones that insects in different feeding guilds, or pathogens with different trophic strategies commonly trigger we predict
the outcome (i.e. inhibition or facilitation) of these plant-mediated indirect interactions.

In the figure, arrow endings represent findings from references discussed in the article.

SA = Salicylic acid, JA = Jasmonic acid, ET = Ethylene, ETI = Effector triggered immunity.

Frago & É. Bauce (2014) Life-history consequences of chronic nutritional stress in an outbreaking insect defoliator.
. PDF.

In February we published a paper exploring 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 & H.C.J. Godfray (2014) Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community. Oecologia. Abstract.

 We studied a food web (a) consisting of two aphid species, the pea aphid (Acyrthosiphon pisum; AP) and the grain aphid (Sitobion avenae; SA) feeding on broad beans (Vicia faba) and wheat (Triticum aestivum), respectively, and two shared natural enemies, the parasitoid (Aphidius ervi; AE) and the seven-spot ladybird (Coccinella septem punctata; CS). Our results (b) suggest that CS cues reduce AE parasitism on AP which in the long term also benefits SA, a case of apparent mutualism. Solid arrows show direct trophic links and dashed arrows depict trait-mediated indirect interactions.

In December 2012 we published a paper where we review recent examples on the role of insect symbionts in insect-plant interactions.
E. Frago, M. Dicke & H.C.J. Godfray (2012) Insect symbionts as hidden players in insect-plant interactions.
Trends in Ecology & Evolution
. Abstract.

This figure depicts some of the interactions we review:
Insect symbionts (represented by an insect carrying a bacterium) influence insect–plant interactions at different levels through direct interactions (solid lines) as well as through indirect plant-mediated interactions (dashed lines). Yellow lines represent symbiont-mediated interactions, deep green lines represent insect–plant interactions, and pale green lines represent changes in plant state or physiology. (a) Insect symbionts can directly influence host plant use in herbivorous insects (A1), but also indirectly through changes to plant state or physiology (A2). Such changes can affect other insects sharing the same host plant (A3). Insect symbionts can directly affect the host’s interactions with natural enemies (A4), but also indirectly through changes in plant physiology and the emission of herbivore-induced plant volatiles (A5). (b) Insect symbionts can colonize plants, which is a likely route for horizontal transmission (B1). Similarly, plant pathogens can be vectored by insects and this may evolve into mutualism if the insect benefits from a diseased host plant (B2). (c) Different insect symbionts can differentially affect insect host plant use and ultimately modulate interactions between insects. (d) Communities of insect symbionts, including bacteria, fungi, and viruses, are found in both insects and plants, where they can engage in complex interactions. 

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.