Helen Hesketh

Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects

The use of fungal entomopathogens as microbial control agents has driven studies into their ecology in crop ecosystems. Yet, there is still a lack of understanding of the ecology of these insect pathogens in semi-natural habitats and communities. We review the literature on prevalence of fungal entomopathogens in insect populations and highlight the difficulties in making such measurements. We then describe the theoretical host-pathogen models available to examine the role that fungal entomopathogens could play in regulating insect populations in semi-natural habitats, much of the inspiration for which has been drawn from managed systems, particularly forests. We further emphasise the need to consider the complexity, and particularly the heterogeneity, of semi-natural habitats within the context of theoretical models and as a framework for empirical studies. We acknowledge that fundamental gaps in understanding fungal entomopathogens from an ecological perspective coupled with a lack of empirical data to test theoretical predictions is impeding progress. There is an increasing need, especially under current rapid environmental change, to improve our understanding of the role of fungi in insect population dynamics beyond the context of forestry and agriculture.

Attraction of Male European Tarnished Plant Bug, Lygus rugulipennis to Components of the Female Sex Pheromone in the Field

Previous work showed that females of the European tarnished plant bug, Lygus rugulipennis Poppius (Heteroptera: Miridae), produced three chemicals, hexyl butyrate, (E)-2-hexenyl butyrate, and (E)-4-oxo-2-hexenal, and that these were suspected to be components of the female sex pheromone. In field experiments, traps baited with blends of these chemicals dispensed from polyethylene vials and sachets failed to catch significant numbers of males. Here, we report more recent field experiments in which the chemicals were released from glass microcapillary tubes. A blend of hexyl butyrate and (E)-4-oxo-2-hexenal was significantly attractive to male L. rugulipennis. In addition, whereas the mixture of all three components attracted fewer L. rugulipennis males, this tertiary blend captured significantly greater numbers of males of the congeneric species Lygus pratensis than the binary mixture. The possible reasons for the success of the microcapillaries compared with other dispensers are discussed.

Beyond biological control: non‐pest insects and their pathogens in a changing world

Abstract. 1 Over the last few decades, there have been considerable advances in the fields of insect pathology and insect conservation but the two disciplines rarely meet. The potential of entomopathogens as biological control agents of pest insects is widely recognised but information on the role of pathogens in insect population regulation, more generally, is limited. For example, the role of pathogens as natural enemies of non‐pest insects, including those of conservation value, is seldom considered beyond their context as ‘non‐targets’ of microbial control agents. 2 Entomopathogens are prevalent in natural systems and should receive greater attention in life‐history studies. There is no doubt that viruses, bacteria and fungi are major mortality agents of insects but their significance tends to be overshadowed by the attention given to predators and parasitoids. 3 We highlight the critical function that entomopathogens could have in insect population dynamics with particular reference fragmented habitats as illustrated by the theoretical literature. However, we emphasise that there are few empirical studies to test theoretical predictions. 4 We suggest that since an increase in the incidence of disease is predicted in most environmental change scenarios, it is more important than ever to turn our attention to insect pathology when we consider insect population dynamics.

Maternal effects, flight versus fecundity trade-offs, and offspring immune defence in the Speckled Wood butterfly, Pararge aegeria.

BackgroundMaternal condition can generate resource-related maternal effects through differential egg provisioning, and can greatly affect offspring performance. In the present study, the speckled wood butterfly Pararge aegeria (L.) was used to investigate whether (after controlling for egg size) maternal age, and increased flight during the oviposition period, resulted in changes in egg provisioning and whether this contributed to variation in offspring performance, i) early in development (egg stage and early post-hatching development), and ii) later in larval development after being exposed to the model viral pathogen system; the baculovirus Autographa californica multinucleocapsid nucleopolyhedrovirus (AcMNPV).ResultsAge-related changes in maternal egg provisioning were observed to influence egg stage development only. Flight-induced changes in maternal egg provisioning had direct consequences for offspring growth and survival across each life stage from egg to adulthood; offspring from forced flight mothers had lower larval masses and longer development times. Offspring with lower larval masses also had reduced survival after exposure to the viral pathogen.ConclusionThe present study demonstrates that a change in maternal provisioning as a result of increased flight during the oviposition period has the potential to exert non-genetic cross-generational fitness effects in P. aegeria. This could have important consequences for population dynamics, particularly in fragmented anthropogenic landscapes.

The common black ant, Lasius niger (Hymenoptera: Formicidae), as a vector of the entomopathogen Lecanicillium longisporum to rosy apple aphid, Dysaphis plantaginea (Homoptera: Aphididae).

The potential for common black ant Lasius niger workers to vector conidia of the entomopathogenic fungus Lecanicillium longisporum to colonies of the rosy apple aphid Dysaphis plantaginea was assessed in laboratory and field experiments. Scanning electron microscope studies showed that L. niger workers which were artificially contaminated with L. longisporum conidia, carried conidia primarily on their tarsae but also on antennae and mandibles. Neither L. niger workers nor larvae were susceptible to infection with L. longisporum. Workers which were artificially contaminated with conidia of L. longisporum initiated infection in colonies of healthy D. plantaginea on apple. Mortality due to L. longisporum was recorded as 68.3, 30.8 and 3.7% of aphids under laboratory, semi-field and field conditions, respectively.

Extending standard testing period in honeybees to predict lifespan impacts of pesticides and heavy metals using dynamic energy budget modelling

Concern over reported honeybee (Apis mellifera spp.) losses has highlighted chemical exposure as a risk. Current laboratory oral toxicity tests in A. mellifera spp. use short-term, maximum 96 hour, exposures which may not necessarily account for chronic and cumulative toxicity. Here, we use extended 240 hour (10 day) exposures to examine seven agrochemicals and trace environmental pollutant toxicities for adult honeybees. Data were used to parameterise a dynamic energy budget model (DEBtox) to further examine potential survival effects up to 30 day and 90 day summer and winter worker lifespans. Honeybees were most sensitive to insecticides (clothianidin > dimethoate ≫ tau-fluvalinate), then trace metals/metalloids (cadmium, arsenic), followed by the fungicide propiconazole and herbicide 2,4-dichlorophenoxyacetic acid (2,4-D). LC50s calculated from DEBtox parameters indicated a 27 fold change comparing exposure from 48 to 720 hours (summer worker lifespan) for cadmium, as the most time-dependent chemical as driven by slow toxicokinetics. Clothianidin and dimethoate exhibited more rapid toxicokinetics with 48 to 720 hour LC50s changes of <4 fold. As effects from long-term exposure may exceed those measured in short-term tests, future regulatory tests should extend to 96 hours as standard, with extension to 240 hour exposures further improving realism.

Comparing bee species responses to chemical mixtures: Common response patterns?

Pollinators in agricultural landscapes can be exposed to mixtures of pesticides and environmental pollutants. Existing mixture toxicity modelling approaches, such as the models of concentration addition and independent action and the mechanistic DEBtox framework have been previously shown as valuable tools for understanding and ultimately predicting joint toxicity. Here we apply these mixture models to investigate the potential to interpret the effects of semi-chronic binary mixture exposure for three bee species: Apis mellifera, Bombus terrestris and Osmia bicornis within potentiation and mixture toxicity experiments. In the potentiation studies, the effect of the insecticide dimethoate with added propiconazole fungicide and neonicotinoid insecticide clothianidin with added tau-fluvalinate pyrethroid acaricide showed no difference in toxicity compared to the single chemical alone. Clothianidin toxicity showed a small scale, but temporally conserved increase in exposure conducted in the presence of propiconazole, particularly for B. terrestris and O. bicornis, the latter showing a near three-fold increase in clothianidin toxicity in the presence of propiconazole. In the mixture toxicity studies, the dominant response patterns were of additivity, however, binary mixtures of clothianidin and dimethoate in A. mellifera, B. terrestris and male O. bicornis there was evidence of a predominant antagonistic interaction. Given the ubiquitous nature of exposures to multiple chemicals, there is an urgent need to consider mixture effects in pollinator risk assessments. Our analyses suggest that current models, particularly those that utilise time-series data, such as DEBtox, can be used to identify additivity as the dominant response pattern and also those examples of interactions, even when small-scale, that may need to be taken into account during risk assessment.

Exploring sub-lethal effects of exposure to a nucleopolyhedrovirus in the speckled wood (Pararge aegeria) butterfly.

This study investigated the sub-lethal effects of larval exposure to baculovirus on host life history and wing morphological traits using a model system, the speckled wood butterfly Pararge aegeria (L.) and the virus Autographa californica nucleopolyhedrovirus. Males and females showed similar responses to the viral infection. Infection significantly reduced larval growth rate, whilst an increase in development time allowed the critical mass for pupation to be attained. There was no direct effect of viral infection on the wing morphological traits examined. There was, however, an indirect effect of resisting infection; larvae that took longer to develop had reduced resource investment in adult flight muscle mass.

Towards a coordination of European activities to diagnose and manage insect diseases in production facilities

The rapid increase in insect production for food and feed both in Europe and elsewhere in the world has led to a need for a coordinated action to assist producers in the diagnosis and management of insect diseases in production stock. Diseases caused by viruses, bacteria, fungi, protozoa and other insect pathogens can be detrimental for reared insects and may cause significant economic loss to producers. Here, we suggest how academia, commercial companies and other insect producers can jointly develop best practice for diagnosing insect diseases early and thereby manage such diseases efficiently. First, we analyse different ways of transmission of insect diseases in closed and semi-closed production facilities. Thereafter we describe four recent cases where companies have requested advice about insect pathogens in their insect stock namely: with giant mealworm Zophobas morio, yellow mealworm Tenebrio molitor, house cricket Acheta domesticus, and with lesser mealworm Alphitobius diaperinus. Our experience dealing with these cases gave us insight to suggest how we should coordinate European activities to establish a service to diagnose and provide advice, and how different European laboratories specialised in insect pathology should collaborate. An important issue will be to educate a new generation of insect pathologists, who with a combination of classical insect pathology methods and the most modern tools can become professionals in diagnosing and managing the various types of insect pathogens.

Viral exposure effects on life-history, flight-related traits, and wing melanisation in the Glanville fritillary butterfly

Graphical abstract