Aggregation of parasitism risk in an aphid-parasitoid system: Effects of plant patch size and aphid density

Few studies have linked density dependence of parasitism and the tritrophic environment within which a parasitoid forages. In the non-crop plant-aphid, Centaurea nigra-Uroleucon jaceae system, mixed patterns of density-dependent parasitism by the parasitoids Aphidius funebris and Trioxys centaureae were observed in a survey of a natural population. Breakdown of density-dependent parasitism revealed that density dependence was inverse in smaller colonies but direct in large colonies (>20 aphids), suggesting there is a threshold effect in parasitoid response to aphid density. The CV2 of searching parasitoids was estimated from parasitism data using a hierarchical generalized linear model, and CV2>1 for A. funebris between plant patches, while for T. centaureae CV2>1 within plant patches. In both cases, density independent heterogeneity was more important than density-dependent heterogeneity in parasitism. Parasitism by T. centaureae increased with increasing plant patch size. Manipulation of aphid colony size and plant patch size revealed that parasitism by A. funebris was directly density dependent at the range of colony sizes tested (50-200 initial aphids), and had a strong positive relationship with plant patch size. The effects of plant patch size detected for both species indicate that the tritrophic environment provides a source of host density independent heterogeneity in parasitism, and can modify density-dependent responses. (c) 2007 Gessellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism

Powdery mildews are phytopathogens whose growth and reproduction are entirely dependent on living plant cells. The molecular basis of this life-style, obligate biotrophy, remains unknown. We present the genome analysis of barley powdery mildew, Blumeria graminis f.sp. hordei (Blumeria), as well as a comparison with the analysis of two powdery mildews pathogenic on dicotyledonous plants. These genomes display massive retrotransposon proliferation, genome-size expansion, and gene losses. The missing genes encode enzymes of primary and secondary metabolism, carbohydrate-active enzymes, and transporters, probably reflecting their redundancy in an exclusively biotrophic life-style. Among the 248 candidate effectors of pathogenesis identified in the Blumeria genome, very few (less than 10) define a core set conserved in all three mildews, suggesting thatmost effectors represent species-specific adaptations.

Organic and conventional fertilizer effects on a tritrophic interaction: parasitism, performance and preference of Cotesia vestalis

Interest in sustainable farming methods that rely on alternatives to conventional synthetic fertilizers and pesticides is increasing. Sustainable farming methods often utilize natural populations of predatory and parasitic species to control populations of herbivores, which may be potential pest species. We investigated the effects of several types of fertilizer, including those typical of sustainable and conventional farming systems, on the interaction between a herbivore and parasitoid. The effects of fertilizer type on percentage parasitism, parasitoid performance, parasitoid attack behaviour and responses to plant volatiles were examined using a model Brassica system, consisting of Brassica oleracea var capitata, Plutella xylostella (Lepidoptera) larvae and Cotesia vestalis (parasitoid). Percentage parasitism was greatest for P. xylostella larvae feeding on plants that had received either a synthetic ammonium nitrate fertilizer or were unfertilized, in comparison to those receiving a composite fertilizer containing hoof and horn. Parasitism was intermediate on plants fertilized with an organically produced animal manure. Male parasitoid tibia length showed the same pattern as percentage parasitism, an indication that offspring performance was maximized on the treatments preferred by female parasitoids for oviposition. Percentage parasitism and parasitoid size were not correlated with foliar nitrogen concentration. The parasitoids did not discriminate between hosts feeding on plants in the four fertilizer treatments in parasitoid behaviour assays, but showed a preference for unfertilized plants in olfactometer experiments. The percentage parasitism and tibia length results provide support for the preference–performance hypothesis

Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids

The effects of arbuscular mycorrhizal colonization of Leucanthemum vulgare on parasitism of a leaf-mining insect was studied in a field and a laboratory experiment. In the field, parasitism of Chromatomyia syngenesiae by Diglyphus isaea was lower on mycorrhizal plants, compared with plants where the association was reduced. A laboratory experiment, in which L. vulgare was inoculated with three species of AM fungi, showed that the effects on parasitism rates were mycorrhizal species-dependent. Some fungal combinations increased parasitism, some decreased it, while others had no effect. It is concluded that the most likely cause of these differences is plant size, with parasitoid searching efficiency being reduced on the larger plants, resulting from certain mycorrhizal species combinations. However, a mycorrhizal effect on herbivore-produced plant volatiles cannot be ruled out.

Differential susceptibilities of peach-potato aphid, Myzus persicae (Homoptera: Aphididae) and its parasitoid, Aphidius matricariae (Hymenoptera: Aphidiidae) to foliar insecticides on partially resistant and susceptible potato cultivars

In a field experiment the effects of Sumicidin (super) 5EC (fenitrothion), Metasystox EC25 (oxydemeton-methyl) and Tamaron SL600 (methamidophos), applied at different dosages, were evaluated against peach-potato aphid, Myzus persicae (Sulzer) and its parasitoid Aphidius matricariae Haliday on Cardinal and Desiree (respectively partially resistant and susceptible potato cultivars to M. persicae). Sumicidin (super) 5EC was found about 30% more effective in reducing aphid populations than the other insecticides tested. The highest doses of each insecticide caused maximum aphid mortality; in general aphid mortality appeared dose dependent. Almost all the higher and lower doses of the tested insecticides were about 19% more effective on Cardinal than on Desiree. The most significant result was the synergistic interaction at the lower doses with plant resistance, so that the same level of control was recorded with second highest dose on Cardinal as with the highest dose on Desiree. Also the same control level was achieved at the lowest dosage rate on Cardinal compared with the next higher dose on the Desiree. Sumicidin (super) 5EC was found least toxic to the parasitoid, A. matricariae in terms of percent parasitism, emergence of parasitoids and number of mature eggs in the emerging female parasitoids; increase of about 22, 67 and 47% respectively were found in parasitoid performance with Tamaron SL600 which was found comparatively highly toxic. The highest doses of all insecticides were found clearly toxic to the parasitoid. In general, effects on the parasitoid were dose dependent. Maximum yield was obtained from the second highest dose of Sumicidin (super) 5EC.

Selective toxicity of different granular insecticides to the peach-potato aphid, Myzus persicae (Homoptera: Aphididae) and its parasitoid, Aphidius matricariae (Hymenoptera: Aphidiidae) in two differentially resistant potato cultivars

Field studies were conducted in Pakistan to examine the effects and the interaction of two differentially resistant potato cultivars i.e. Cardinal and Desiree (one partially resistant and one susceptible to Myzus persicae (Sulzer), respectively) with different dosage rates of granular insecticides, at different time intervals after application in relation to percent kill of M. persicae and effects on the parasitoid Aphidius matricariae Haliday (i.e. the third trophic level) within the aphid mummies, percent parasitism and Thimet 10G (phorate) was found about 30% more effective in reducing aphid population than the Furadan 3G (carbofuran). The highest doses of each insecticide caused maximum aphid mortality, in general aphid mortality appeared dose dependent. Mostly all the higher and lower doses of the tested insecticides were about 10% more effective on Cardinal than on Desiree. The most significant result was the synergistic interaction at the lower doses with plant resistance, so that the same level of control was recorded with the second highest dose on Cardinal as with the highest dose on Desiree. Also the same level of control was observed at the lowest dose on Cardinal as with the second last lowest dose on Desiree. Furadan 3G was found least toxic to the A. matricariae in terms of percent parasitism, emergence of parasitoids and number of mature eggs in the emerging females. Furadan 3G gave 13, 15 and 6% higher figures, respectively from the parasitoid characteristics than Thimet 10G. The highest doses of both insecticides were clearly toxic to the parasitoid. In general, the effects on the parasitoid were dose dependent. The second highest dose of Thimet 10G, gave the maximum yield

Drought stress differentially affects leaf-mining species

1. The impact of climate change on phytophages is difficult to predict, due in part to variation between species in their responses to factors such as drought stress. Here, the hypothesis that several species within the leaf-mining feeding guild will respond in a consistent way to changes in rainfall patterns is tested, using a manipulative field experiment. 2. Summer drought, enhanced summer rainfall, and control treatments were imposed on a calcareous grassland community, and the responses of five leaf-mining species were assessed. 3. One leaf-mining species was more abundant under enhanced rainfall, one was more abundant under drought, and the other three species showed no consistent response to the rainfall treatments. Higher parasitism levels under drought may partly explain the response of one species (Stephensia brunnichella) to the treatments. 4. These results show that generalisations relating to drought stress impacts cannot be drawn at the feeding guild level for leaf-mining insects.

Summer drought alters plant-mediated competition between foliar- and root-feeding insects

Summer droughts are predicted to increase in severity and frequency in the United Kingdom, due to climate change. Few studies have addressed the impacts of drought on interactions between species, and the majority have focussed on increases in CO2 concentration and changes in temperature. Here, the effect of experimental summer drought on the strength of the plant-mediated interaction between leaf-mining Stephensia brunnichella larvae and root-chewing Agriotes larvae was investigated. Agriotes larvae reduced the abundance and performance of S. brunnichella feeding on a mutual host plant, Clinopodium vulgare, as well as the rate of parasitism of the leaf-miner. The interaction did not, however, occur on plants subjected to a severe drought treatment, which were reduced in size. Changes to summer rainfall, due to climate change, may therefore reduce the occurrence of plant-mediated interactions between insect herbivores.

The impact of Rhinanthus minor in newly established meadows on a productive site

Question: What is the impact of the presence of Rhinanthus minor on forb abundance in newly established swards? Location: Wetherby, West Yorkshire, UK (53 degrees 55' N, 1 degrees 22(1) W). Method: A standard meadow mix containing six forbs and six grasses was sown on an ex-arable field and immediately over-sown using a randomised plot design with three densities of Rhinanthus minor (0, 600, and 1000 seeds per m(2)). Above-ground biomass was analysed over a period of three years, while detailed assessments of sward composition were performed during the first two years. Results: Values of grass biomass were reduced in the presence of Rhinanthus, especially at the higher sowing density. The ratio of grass: forb biomass was also lower in association with Rhinanthus, but only at the higher sowing density. The presence of Rhinanthus, had no effect on species number or diversity, which decreased between years regardless of treatment. Conclusions: Although not tested in a multi-site experiment, the benefit of introducing Rhinanthus into newly established swards to promote for abundance was determined. The efficacy of Rhinanthus presence is likely to depend on whether species not susceptible to the effects of parasitism are present.

Tolerance traits and the stability of mutualism

Identifying factors which allow the evolution and persistence of cooperative interactions between species is a fundamental issue in evolutionary ecology. Various hypotheses have been suggested which generally focus on mechanisms that allow cooperative genotypes in different species to maintain interactions over space and time. Here, we emphasise the fact that even within mutualisms (interactions with net positive fitness effects for both partners), there may still be inherent costs, such as the occasional predation by ants upon aphids. Individuals engaged in mutualisms benefit from minimising these costs as long as it is not at the expense of breaking the interspecific interaction, which offers a net positive benefit. The most common and obvious defence traits to minimise interspecific interaction costs are resistance traits, which act to reduce encounter rate between two organisms. Tolerance traits, in contrast, minimise fitness costs to the actor, but without reducing encounter rate. Given that, by definition, it is beneficial to remain in mutualistic interactions, the only viable traits to minimise costs are tolerance-based 'defence' strategies. Thus, we propose that tolerance traits are an important factor promoting stability in mutualisms. Furthermore, because resistance traits tend to propagate coevolutionary arms races between antagonists, whilst tolerance traits do not, we also suggest that tolerance-based defence strategies may be important in facilitating the transition from antagonistic interactions into mutualisms. For example, the mutualism between ants and aphids has been suggested to have evolved from parasitism. We describe how phenotypic plasticity in honeydew production may be a tolerance trait that has prevented escalation into an antagonistic arms race and instead led to mutualistic coevolution.

Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps

Diversification of insect herbivores is often associated with coevolution between plant toxins and insect countermeasures, resulting in a specificity that restricts host plant shifts. Gall inducers, however, bypass plant toxins and the factors influencing host plant associations in these specialized herbivores remain unclear. We reconstructed the evolution of host plant associations in Western Palaearctic oak gallwasps (Cynipidae: Cynipini), a species-rich lineage of specialist herbivores on oak (Quercus). (1) Bayesian analyses of sequence data for three genes revealed extreme host plant conservatism, with inferred shifts between major oak lineages (sections Cerris and Quercus) closely matching the minimum required to explain observed diversity. It thus appears that the coevolutionary demands of gall induction constrain host plant shifts, both in cases of mutualism (e.g., fig wasps, yucca moths) and parasitism (oak gallwasps). (2) Shifts between oak sections occurred independently in sexual and asexual generations of the gallwasp lifecycle, implying that these can evolve independently. (3) Western Palaearctic gallwasps associated with sections Cerris and Quercus diverged at least 20 million years ago (mya), prior to the arrival of oaks in the Western Palaearctic from Asia 5-7 mya. This implies an Asian origin for Western Palaearctic gallwasps, with independent westwards range expansion by multiple lineages.

The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa)

The myxozoan, Tetracapsuloides bryosalmonae, exploits freshwater bryozoans as definitive hosts, occurring as cryptic stages in bryozoan colonies during covert infections and as spore-forming sacs during overt infections. Spores released from sacs are infective to salmonid fish, causing the devastating Proliferative Kidney Disease (PKD). We undertook laboratory studies using mesocosm systems running at 10, 14 and 20 degrees C to determine how infection by T bryosalmonae and water temperature influence fitness of one of its most important bryozoan hosts, Fredericella sultana, over a period of 4 weeks. The effects of infection were context-dependent and often undetectable. Covert infections appear to pose very low energetic costs. Thus, we found that growth of covertly infected F. sultana colonies was similar to that of uninfected colonies regardless of temperature, as was the propensity to produce dormant resting stages (statoblasts). Production of statoblasts, however, was associated with decreased growth. Overt infections imposed greater effects on correlates of host fitness by: (i) reducing growth rates at the two higher temperatures: (ii) increasing mortality rates at the highest temperature: (iii) inhibiting statoblast production. Our results indicate that parasitism should have a relatively small effect on host fitness in the field as the negative effects of infection were mainly expressed in environmentally extreme conditions (20 degrees C for 4 weeks). The generally low virulence of T. bryosalmonae is similar to that recently demonstrated for another myxozoan endoparasite of freshwater bryozoans. The unique opportunity for extensive vertical transmission in these colonial invertebrate hosts couples the reproductive interests of host and parasite and may well give rise to the low virulence that characterises these systems. Our study implies that climate change can be expected to exacerbate PKD outbreaks and increase the geographic range of PKD as a result of the combined responses of T. bryosalmonae and its bryozoan hosts to higher temperatures. Crown Copyright (C) 2009 Published by Elsevier Ltd. All rights reserved.

A role for parasites in stabilising the fig-pollinator mutualism

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their "fruits'' (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.

When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants

Most studies aiming to determine the beneficial effect of ants on plants simply consider the effects of the presence or exclusion of ants on plant yield. This approach is often inadequate, however, as ants interact with both non-tended herbivores and tended Homoptera. Moreover, the interaction with these groups of organisms is dependent on ant density, and these functional relationships are likely to be non-linear. A model is presented here that segregates plant herbivores into two categories depending on the sign of their numerical response to ants (myrmecophiles increase with ants, non-tended herbivores decline). The changes in these two components of herbivores with increasing ant density and the resulting implications for ant-plant mutualisms are considered. It emerges that a wide range of ant densities needs to be considered as the interaction sign (mutualism or parasitism) and strength is likely to change with ant density. The model is used to interpret the results of an experimental study that varied levels of Aphis fabae infestation and Lasius niger ant attendance on Vicia faba bean plants. Increasing ant density consistently reduced plant fitness and thus, in this location, the interaction between the ants and the plant can be considered parasitic. In the Vicia faba system, these costs of ants are unlikely to be offset by other beneficial agents (e.g., parasitoids), which also visit extrafloral nectaries.

Control of Leveillula taurica in tomato by Acremonium alternatum is by induction of resistance, not Hyperparasitism

Spores of the hyperparasite Acremonium alternatum reduced powdery mildew infection by Leveillula taurica on greenhouse tomato. The effect was slightly increased when spores were applied killed, and therefore not due to direct parasitism. The effect was systemic, protecting untreated leaves above the treated ones. Spores killed by heat had more effect than when killed by UV, so the effect was presumably due to induction of host resistance by substances released when cells were heat killed. The size of the effect depended upon leaf age and level of infection. Effects on primary infection and expansion of successful infections appear to be under independent control.