Herbivore-induced plant volatiles, not natural enemies, mediate a positive indirect interaction between insect herbivores.

Many insect herbivores engage in apparent competition whereby two species interact through shared natural enemies. Upon insect attack, plants release volatile blends that attract natural enemies, but whether these volatiles mediate apparent competition between herbivores is not yet known. We investigate the role of volatiles that are emitted by bean plants upon infestation by Acyrthosiphon pisum aphids on the population dynamics and fitness of Sitobion avenae aphids, and on wheat phloem sap metabolites. In a field experiment, the dynamics of S. avenae aphids on wheat were studied by crossing two treatments: exposure of aphid colonies to A. pisum-induced bean volatiles and exclusion of natural enemies. Glasshouse experiments and analyses of primary metabolites in wheat phloem exudates were performed to better understand the results from the field experiment. In the field, bean volatiles did not affect S. avenae dynamics or survival when aphids were exposed to natural enemies. When protected from them, however, volatiles led to larger aphid colonies. In agreement with this observation, in glasshouse experiments, aphid-induced bean volatiles increased the survival of S. avenae aphids on wheat plants, but not on an artificial diet. This suggests that volatiles may benefit S. avenae colonies via metabolic changes in wheat plants, although we did not find any effect on wheat phloem exudate composition. We report a potential case of associational susceptibility whereby plant volatiles weaken the defences of receiving plants, thus leading to increased herbivore performance.

Multiple phenotypes conferred by a single insect symbiont are independent.

Many microbial symbionts have multiple phenotypic consequences for their animal hosts. However, the ways in which different symbiont-mediated phenotypes combine to affect fitness are not well understood. We investigated whether there are correlations between different symbiont-mediated phenotypes. We used the symbiont Spiroplasma, a striking example of a bacterial symbiont conferring diverse phenotypes on insect hosts. We took 11 strains of Spiroplasma infecting pea aphids (Acyrthosiphon pisum) and assessed their ability to provide protection against the fungal pathogen Pandora neoaphidis and the parasitoids Aphidius ervi and Praon volucre. We also assessed effects on male offspring production for five of the Spiroplasma strains. All but one of the Spiroplasma strains provided very strong protection against the parasitoid P. volucre. As previously reported, variable protection against P. neoaphidis and A. ervi was also present; male-killing was likewise a variable phenotype. We find no evidence of any correlation, positive or negative, between the different phenotypes, nor was there any evidence of an effect of symbiont phylogeny on protective phenotype. We conclude that multiple symbiont-mediated phenotypes can evolve independently from one another without trade-offs between them.

Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont.

Many insects harbour facultative endosymbiotic bacteria, often more than one type at a time. These symbionts can have major effects on their hosts' biology, which may be modulated by the presence of other symbiont species and by the host's genetic background. We investigated these effects by transferring two sets of facultative endosymbionts (one Hamiltonella and Rickettsia, the other Hamiltonella and Spiroplasma) from naturally double-infected pea aphid hosts into five novel host genotypes of two aphid species. The symbionts were transferred either together or separately. We then measured aphid fecundity and susceptibility to an entomopathogenic fungus. The pathogen-protective phenotype conferred by the symbionts Rickettsia and Spiroplasma varied among host genotypes, but was not influenced by co-infection with Hamiltonella. Fecundity varied across single and double infections and between symbiont types, aphid genotypes and species. Some host genotypes benefit from harbouring more than one symbiont type.

Effects of bacterial secondary symbionts on host plant use in pea aphids.

Aphids possess several facultative bacterial symbionts that have important effects on their hosts' biology. These have been most closely studied in the pea aphid (Acyrthosiphon pisum), a species that feeds on multiple host plants. Whether secondary symbionts influence host plant utilization is unclear. We report the fitness consequences of introducing different strains of the symbiont Hamiltonella defensa into three aphid clones collected on Lathyrus pratensis that naturally lack symbionts, and of removing symbionts from 20 natural aphid-bacterial associations. Infection decreased fitness on Lathyrus but not on Vicia faba, a plant on which most pea aphids readily feed. This may explain the unusually low prevalence of symbionts in aphids collected on Lathyrus. There was no effect of presence of symbiont on performance of the aphids on the host plants of the clones from which the H. defensa strains were isolated. Removing the symbiont from natural aphid-bacterial associations led to an average approximate 20 per cent reduction in fecundity, both on the natural host plant and on V. faba, suggesting general rather than plant-species-specific effects of the symbiont. Throughout, we find significant genetic variation among aphid clones. The results provide no evidence that secondary symbionts have a major direct role in facilitating aphid utilization of particular host plant species.

An age-structured model to evaluate the potential of novel malaria-control interventions: a case study of fungal biopesticide sprays.

It has recently been proposed that mosquito vectors of human diseases, particularly malaria, may be controlled by spraying with fungal biopesticides that increase the rate of adult mortality. Though fungal pathogens do not cause instantaneous mortality, they can kill mosquitoes before they are old enough to transmit disease. A model is developed (i) to explore the potential for fungal entomopathogens to reduce significantly infectious mosquito populations, (ii) to assess the relative value of the many different fungal strains that might be used, and (iii) to help guide the tactical design of vector-control programmes. The model follows the dynamics of different classes of adult mosquitoes with the risk of mortality due to the fungus being assumed to be a function of time since infection (modelled using the Weibull distribution). It is shown that substantial reductions in mosquito numbers are feasible for realistic assumptions about mosquito, fungus and malaria biology and moderate to low daily fungal infection probability. The choice of optimal fungal strain and spraying regime is shown to depend on local mosquito and malaria biology. Fungal pathogens may also influence the ability of mosquitoes to transmit malaria and such effects are shown to further reduce vectorial capacity.

The population genetics of using homing endonuclease genes in vector and pest management.

Homing endonuclease genes (HEGs) encode proteins that in the heterozygous state cause double-strand breaks in the homologous chromosome at the precise position opposite the HEG. If the double-strand break is repaired using the homologous chromosome, the HEG becomes homozygous, and this represents a powerful genetic drive mechanism that might be used as a tool in managing vector or pest populations. HEGs may be used to decrease population fitness to drive down population densities (possibly causing local extinction) or, in disease vectors, to knock out a gene required for pathogen transmission. The relative advantages of HEGs that target viability or fecundity, that are active in one sex or both, and whose target is expressed before or after homing are explored. The conditions under which escape mutants arise are also analyzed. A different strategy is to place HEGs on the Y chromosome that cause one or more breaks on the X chromosome and so disrupt sex ratio. This strategy can cause severe sex-ratio biases with efficiencies that depend on the details of sperm competition and zygote mortality. This strategy is probably less susceptible to escape mutants, especially when multiple X shredders are used.

Selection for resistance to a fungal pathogen in Drosophila melanogaster.

An artificial selection experiment designed to explore the evolution of resistance to a fungal pathogen, Beauveria bassiana, in Drosophila melanogaster is reported here. The experiment was designed to test whether there is sufficient additive genetic variation in this trait for increased resistance to evolve, and, if so, whether there are correlated responses that might represent a cost to defence. After 15 generations of selection, flies from selected lines did not have higher overall fitness after infection compared with control lines. The response to selection for resistance against this pathogen is thus much weaker than against other species, in particular, parasitoids. There was, however, evidence for increased late-life fecundity in selected lines, which may indicate evolved tolerance of fungal infection. This increase was accompanied by reduced early-life fitness, which may reflect the well-known trade-off between early and late reproduction. In the absence of fungal infection, selected flies had lower fitness than control flies, and the possibility that this is also a trade-off with increased tolerance is explored.

Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids.

1. Most communities of insect herbivores are unlikely to be structured by resource competition, but they may be structured by apparent competition mediated by shared natural enemies. 2. The potential of three guilds of natural enemies (parasitoids, fungal entomopathogens and predators) to influence aphid community structure through indirect interactions is assessed. Based on the biology, we predicted that the scope for apparent competition would be greatest for the predator and least for the parasitoid guilds. 3. Separate fully quantitative food webs were constructed for 3 years for the parasitoid guild, 2 years for the pathogen guild and for a single year for the predator guild. The webs were analysed using standard food web statistics designed for binary data, and using information-theory-based metrics that make use of the full quantitative data. 4. A total of 29 aphid, 24 parasitoid, five entomopathogenic fungi and 13 aphid specialist predator species were recorded in the study. Aphid density varied among years, and two species of aphid were particularly common in different years. Omitting these species, aphid diversity was similar among years. 5. The parasitoid web showed the lowest connectance while standard food web statistics suggested the pathogen and predator webs had similar levels of connectance. However, when a measure based on quantitative data was used the pathogen web was intermediate between the other two guilds. 6. There is evidence that a single aphid species had a particularly large effect on the structure of the pathogen food web. 7. The predator and pathogen webs were not compartmentalized, and the vast majority of parasitoids were connected in a single large compartment. 8. It was concluded that indirect effects are most likely to be mediated by predators, a prediction supported by the available experimental evidence.

Phylogenetic analysis of trophic associations.

Ecologists frequently collect data on the patterns of association between adjacent trophic levels in the form of binary or quantitative food webs. Here, we develop statistical methods to estimate the roles of consumer and resource phylogenies in explaining patterns of consumer-resource association. We use these methods to ask whether closely related consumer species are more likely to attack the same resource species and whether closely related resource species are more likely to be attacked by the same consumer species. We then show how to use estimates of phylogenetic signals to predict novel consumer-resource associations solely from the phylogenetic position of species for which no other (or only partial) data are available. Finally, we show how to combine phylogenetic information with information about species' ecological characteristics and life-history traits to estimate the effects of species traits on consumer-resource associations while accounting for phylogenies. We illustrate these techniques using a food web comprising species of parasitoids, leaf-mining moths, and their host plants.

Learning, Host Fidelity, and the Stability of Host-Parasitoid Communities.

Simple models of host-parasitoid interactions show that a polyphagous parasitoid tends to drive extinct all but the most fecund of its hosts. Coexistence requires a mechanism by which hosts with lower fecundity can increase when rare. We explore how recently discovered parasitoid learning behavior can contribute to species coexistence. On emergence as adults, parasitoids learn chemical cues associated with their natal host and hence are more likely to locate and to oviposit in hosts of the same species. For two models incorporating different assumptions about parasitoid searching, we derive conditions for the strength of host fidelity that permits a feasible multihost equilibrium and argue that this equilibrium is stable whenever the corresponding single-host equilibria are stable.

Geographic Patterns in the Evolution of Resistance and Virulence in Drosophila and Its Parasitoids.

Many insects are attacked by internal parasitoids against which they mount a largely cellular immunological defense. The resistance of a host and the virulence of a parasitoid determine which species survives after parasitism. Drosophila is parasitized by several hymenopterous parasitoids, especially those in the genera Asobara and Leptopilina. Geographic patterns have been found in parasitoid virulence and host resistance, the clearest of which is a cline in Asobara tabida virulence from the north (low) to the south (high) of Europe. Drosophila melanogaster resistance is highest in central-southern Europe and lower elsewhere. We review and interpret these patterns in the light of recent experimental and theoretical studies of the evolution and coevolution of these traits. We find no evidence for genotype-specific virulence and defense, which makes "Red Queen"-type coevolution unlikely. The most important explanation for the patterns is geographic differences in host-parasitoid community structure. Asobara tabida virulence is positively correlated with the resistance of its main hosts, and there is more limited evidence that D. melanogaster resistance is influenced by the virulence of its parasitoids. We critically appraise whether the evidence available so far supports a coevolutionary explanation for the levels of these traits.

Mixed sex allocation strategies in a parasitoid wasp.

The sex allocation strategy of the parasitoid Laelius pedatus (Hymenoptera: Bethylidae) on different-sized hosts was investigated. The wasp lays from one to five eggs, and clutch size increases with host size. On the smallest hosts, single male eggs are laid, while on slightly larger hosts single female eggs are laid. On still larger hosts, gregarious clutches are laid which nearly always consist of a single male and one or more female eggs. The sex ratio strategy of the wasp appears to be influenced by a combination of local mate competition and conditional sex expression based on host quality.

The consequences of clustering by Aphis fabae foundresses on spring migrant production.

Aphis fabae (Homoptera: Aphididae) foundresses were shown to have a clustered distribution on leaves of their primary host, Euonymus europaeus. Two field experiments were carried out to determine the costs or benefits of this clustering behaviour to aphid clones. The first experiment, in spring 1996, excluded predators from colonies formed by single fundatrices or clusters of three. No density-dependent effects on colony growth were observed early in the season, but the total production of migrants per foundress was significantly lower for clustered foundresses. This demonstrated that there was no synergistic effect of group feeding on clonal performance. All colonies were initiated on randomly selected leaves and all grew successfully, therefore clustering was not due to a shortage of feeding sites. The second experiment, in spring 1997, tested whether natural enemies cause selection for selfish herding by the foundress generation. Colonies were initiated by one or three foundresses, but half were left unbagged. If natural enemy attack is a selective force inducing clustering behaviour in foundresses, the costs of clustering should have been reduced or negated in unbagged colonies. Colonies grown from clusters produced significantly fewer migrants per foundress, irrespective of bagging treatment. Other potential factors causing clustering behaviour are discussed.

Predators and mutualists influence the exclusion of aphid species from natural communities.

We investigated why two species of aphids (Aphis jacobaeae and Brachycaudus cardui) were very rare in a study site despite their abundance in the surrounding area. The study site contained many common species of aphid and we tested the hypothesis that the community of aphid predators in the field excluded the missing species. Colonies of the two aphid species were artificially initiated in the experimental site and allocated to one of four treatments: control; ground predator exclusion; total predator exclusion, and provision of mutualist ants. Two measures of colony performance were analysed: longevity and cumulative aphid density. Colonies decline naturally in late summer but control colonies disappeared very quickly while colonies protected from all predators survived the longest. The performance of colonies protected from just ground predators was intermediate. We failed to persuade ants to tend A. jacobaeae. Colonies of B. cardui attended by ants performed better than controls and those with ground predators excluded, but not as well as those with all predators excluded. We conclude that the absence of the two species of aphid in the study site is influenced by the resident predator community, and by the availability of mutualists.

Relative movement patterns of a tephritid fly and its parasitoid wasps.

The extent of within-patch dispersal by a tephritid fly and its four major parasitoids was examined over three field seasons. Hosts and parasitoids were marked using acrylic paint and observed as they oviposited into the flowerheads of marsh thistle, Cirsium palustre. The average recapture rate pooled across all species was 22%. The four parasitoids showed consistently greater rates of movement than the host in all three years. In nearly all comparisons, male dispersal was less than female dispersal. There was no evidence that parasitoids moved longer distances after visiting low quality rather than high quality patches. In the one season it was studied, no correlations between movement and insect size were observed. The relevance of these observations to host-parasitoid population dynamics is discussed.

The small-scale spatial distribution of an invading moth.

We studied the spread of a small leaf-mining moth [Phyllonorycter leucographella (Zeller), Gracillariidae] after its accidental introduction into the British Isles. At large geographical scales, previous work had shown the spread to be well described by a travelling weve of constant velocity. Here, we report the pattern of spread at scales of 1 km2. By locating all bushes of the insect's foodplant (Pyracantha spp.) within 1-km2 quadrats, the precise pattern of colonisation at finer spatial scales could be established. Where the 1-km2 site was colonised by moths from the main advancing front, no spatial pattern in the order that bushes were infested was found. If the source of colonisation was a single or small group of infested plants within the site, there was some evidence that nearby plants were colonised first. We found no evidence of population turnover after colonisation. We interpret the results in terms of a two-stage model of invasion that produces different patterns at small and large geographical scales.

The consequence of tree pests and diseases for ecosystem services.

Trees and forests provide a wide variety of ecosystem services in addition to timber, food, and other provisioning services. New approaches to pest and disease management are needed that take into account these multiple services and the different stakeholders they benefit, as well as the likelihood of greater threats in the future resulting from globalization and climate change. These considerations will affect priorities for both basic and applied research and how trade and phytosanitary regulations are formulated.