Joanna T. Staley

Aphids in a changing world: testing the plant stress, plant vigour and pulsed stress hypotheses

1 The plant stress, plant vigour and pulsed stress hypotheses describe the relationships between drought stress, plant quality and herbivore performance. We used an aphid‐Brassica system to test these hypotheses under different drought treatments. 2 The quantity of water added per plant/week was 75%, 50% and 25% of the control (unstressed) water regime for low, medium and high drought stress, respectively, and 50% applied fortnightly for pulsed drought stress. The performance of a ‘senescence’ (generalist) and a ‘flush’ feeder (specialist) aphid species and host plant quality were assessed. 3 Drought treatments had a similar effect on the fecundity and intrinsic rate of increase of both aphid species. Aphid performance on unstressed and highly drought‐stressed plants was significantly lower compared with medium drought stress. On average, 20% greater fecundity and 40% greater intrinsic rates of increase were recorded for both aphid species at medium drought stress compared with unstressed plants. 4 Plant biomass and relative water contents were significantly greater for unstressed plants compared with high and pulsed drought treatments. Foliar nitrogen concentration was significantly greater in the high drought stress and pulsed treatments, and the dominant glucosinolate (glucobrassicin) concentration was significantly greater in drought stress treatments. 5 The present study supports the plant stress hypothesis, although the plant vigour and pulsed stress hypotheses are not supported by our data. The implications of these findings for plant–herbivore interactions under changing environmental conditions are discussed.

Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments

The hypothesis that plants supplied with organic fertilizers are better defended against insect herbivores than those supplied with synthetic fertilizers was tested over two field seasons. Organic and synthetic fertilizer treatments at two nitrogen concentrations were supplied to Brassica plants, and their effects on the abundance of herbivore species and plant chemistry were assessed. The organic treatments also differed in fertilizer type: a green manure was used for the low-nitrogen treatment, while the high-nitrogen treatment contained green and animal manures. Two aphid species showed different responses to fertilizers: the Brassica specialist Brevicoryne brassicae was more abundant on organically fertilized plants, while the generalist Myzus persicae had higher populations on synthetically fertilized plants. The diamondback moth Plutella xylostella (a crucifer specialist) was more abundant on synthetically fertilized plants and preferred to oviposit on these plants. Glucosinolate concentrations were up to three times greater on plants grown in the organic treatments, while foliar nitrogen was maximized on plants under the higher of the synthetic fertilizer treatments. The varying response of herbivore species to these strong differences in plant chemistry demonstrates that hypotheses on defence in organically grown crops have over-simplified the response of phytophagous insects.

Drought and root herbivory interact to alter the response of above-ground parasitoids to aphid infested plants and associated plant volatile signals

Multitrophic interactions are likely to be altered by climate change but there is little empirical evidence relating the responses of herbivores and parasitoids to abiotic factors. Here we investigated the effects of drought on an above/below-ground system comprising a generalist and a specialist aphid species (foliar herbivores), their parasitoids, and a dipteran species (root herbivore).We tested the hypotheses that: (1) high levels of drought stress and below-ground herbivory interact to reduce the performance of parasitoids developing in aphids; (2) drought stress and root herbivory change the profile of volatile organic chemicals (VOCs) emitted by the host plant; (3) parasitoids avoid ovipositing in aphids feeding on plants under drought stress and root herbivory. We examined the effect of drought, with and without root herbivory, on the olfactory response of parasitoids (preference), plant volatile emissions, parasitism success (performance), and the effect of drought on root herbivory. Under drought, percentage parasitism of aphids was reduced by about 40–55% compared with well watered plants. There was a significant interaction between drought and root herbivory on the efficacy of the two parasitoid species, drought stress partially reversing the negative effect of root herbivory on percent parasitism. In the absence of drought, root herbivory significantly reduced the performance (e.g. fecundity) of both parasitoid species developing in foliar herbivores. Plant emissions of VOCs were reduced by drought and root herbivores, and in olfactometer experiments parasitoids preferred the odour from well-watered plants compared with other treatments. The present work demonstrates that drought stress can change the outcome of interactions between herbivores feeding above- and below-ground and their parasitoids, mediated by changes in the chemical signals from plants to parasitoids. This provides a new insight into how the structure of terrestrial communities may be affected by drought.

Growth and defence in young pine and spruce and the expression of resistance to a stem-feeding weevil

Defence in young trees has been much less studied than defence in older ones. In conifers, resin within ducts in bark is an important quantitative defence, but its expression in young trees may be influenced by developmental or physical constraints on the absolute size of the resin ducts as well as by differential allocation of resources to growth and resin synthesis. To examine these relationships, we used nitrogen fertilisation of 1- and 2-year-old pine and spruce to produce trees of different sizes and measured the effect on the number and size of resin ducts and the amount of resin they contained. All of these variables tended to increase with stem diameter, indicating a positive relationship between resin-based defence and growth of 1- and 2-year-old trees. In pine, however, the mass of resin flowing from severed ducts was much lower relative to duct area in 1- than in 2-year-old trees, suggesting that the older trees allocated a higher proportion of the carbon budget to resin synthesis. Resin-based defence in 1-year-old pines appears to be both positively related to growth and resource limited. In spruce, resin production was generally lower, and age-related differences were not observed, suggesting that resin-based defence is less important in this species. Bio-assays of 2-year-old trees with the pine weevil, Hylobius abietis, emphasised the importance of resin as a defence against this bark feeding insect. Nitrogen fertilisation had a limited influence on resistance expression. One-year-old trees remained susceptible because of their small size, low resin production and limited response to fertilisation. The strong growth response of 2-year-old trees to fertilisation increased resin-based defence, but most spruce trees remained susceptible, while most pines were resistant at all levels of fertilisation.

Plant nutrient supply determines competition between phytophagous insects.

Indirect competition is often mediated by plant responses to herbivore feeding damage and is common among phytophagous insect species. Plant-mediated responses may be altered by abiotic conditions such as nutrient supply, which can affect plant growth, morphology, and the concentration of primary and secondary metabolites. Nutrient supply can be manipulated by the type and amount of fertilizer applied to a plant. Brassica oleracea plants were grown in several types of fertilizer, including those commonly used in sustainable and conventional agricultural systems. The occurrence of indirect competition between two phytophagous species from different feeding guilds (a phloem-feeder and leaf-chewer) was assessed. The leaf-chewer reduced aphid populations on plants growing in most fertilizer treatments, but not on those in the ammonium nitrate fertilizer treatment, which caused the highest concentration of foliar nitrogen. The potential consequences of our findings are discussed for phytophagous species in conventional and sustainable agricultural systems.

Effects of organic and conventional fertilizer treatments on host selection by the aphid parasitoid Diaeretiella rapae

The type and quantity of fertilizer supplied to a crop will differ between organic and conventional farming practices. Altering the type of fertilizer a plant is provided with can influence a plant’s foliar nitrogen levels, as well as the composition and concentration of defence compounds, such as glucosinolates. Many natural enemies of insect herbivores can respond to headspace volatiles emitted by the herbivores’ host plant in response to herbivory. We propose that manipulating fertilizer type may also influence the headspace volatile profiles of plants, and as a result, the tritrophic interactions that occur between plants, their insect pests and those pests’ natural enemies. Here, we investigate a tritrophic system consisting of cabbage plants, Brassica oleracea, a parasitoid, Diaeretiella rapae, and one of its hosts, the specialist cabbage aphid Brevicoryne brassicae. Brassica oleracea plants were provided with either no additional fertilization or one of three types of fertilizer: Nitram (ammonium nitrate), John Innes base or organic chicken manure. We investigated whether these changes would alter the rate of parasitism of aphids on those plants and whether any differences in parasitism could be explained by differences in attractivity of the plants to D. rapae or attack rate of aphids by D. rapae. In free‐choice experiments, there were significant differences in the percentage of B. brassicae parasitized by D. rapae between B. oleracea plants grown in different fertilizer treatments. In a series of dual‐choice Y‐tube olfactometry experiments, D. rapae females discriminated between B. brassicae‐infested and undamaged plants, but parasitoids did not discriminate between similarly infested plants grown in different fertilizer treatments. Correspondingly, in attack rate experiments, there were no differences in the rate that D. rapae attacked B. brassicae on B. oleracea plants grown in different fertilizer treatments. These findings are of direct relevance to sustainable and conventional farming practices.

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.

Moth communities and agri-environment schemes: Examining the effects of hedgerow cutting regime on diversity, abundance, and parasitism

Hedgerows provide an important habitat for wildlife including invertebrates, representing a large proportion of semi‐natural habitat patches in the modern agricultural landscapes of the UK and Europe. Around 40% of hedgerow length in England is managed under agri‐environment scheme (AES) options, which specify less frequent cutting and advise cutting in winter. Hedgerow management can alter habitat structure and quality, potentially influencing invertebrate community structure. We assessed the impacts of management treatments on moth communities and their parasitoids. Two treatments (‘cutting frequency’: once every 1, 2, or 3 years, and ‘cutting time’: autumn vs. winter) were applied to a long‐running hedgerow experiment, mimicking AES prescriptions. Moth larvae were collected from the hedgerows, identified and reared to determine parasitism. Hedgerow structure and foliar quality were quantified and related to changes in moth abundance, diversity, species richness, and parasitism. Hedgerow management did not significantly affect overall abundance of moth larvae, but did affect the abundance of certain feeding guilds and trophic interactions with parasitoids. Concealed moth larvae (mining, tentiform, and case bearing) were more abundant on hedgerows cut infrequently (every 2 or 3 years vs. annually). Parasitism rates were higher on hedgerows cut less often, when these were cut in autumn. There was a strong trend towards greater moth species richness and diversity on winter cut hedgerows. Agri‐environment scheme management can thus have complex effects on invertebrate communities. The abundance of some moths may be positively affected by AES hedgerow management and this can have knock‐on effects on parasitoid abundance.

Maternal host plant effects on aphid performance: contrasts between a generalist and a specialist species on Brussels sprout cultivars

1 The performance of the second generation (G2) of alates and apterae of a generalist, Myzus persicae, and a specialist, Brevicoryne brassicae, aphid species reared on Chinese cabbage or cabbage was evaluated on five cultivars of Brussels sprout. 2 Aphid performance was influenced both by the type of host on which the parent aphid had been reared and by the host on which it was feeding when reproducing. 3 The fecundity of the G2 of alates of both aphid species reared on Chinese cabbage differed significantly between all the cultivars of Brussels sprout and, on average, was 25% higher than those reared on cabbage. These differences were also apparent for the intrinsic rate of increase of B. brassicae but not for M. persicae. 4 There was a trend for the G2 of alates from Chinese cabbage to have greater fecundity compared with aphids from cabbage. These differences were significant for the fecundity of the G2 of alates of both aphid species on Brussels sprout cultivars Fillbasket (30% higher), Red Delicious (35% higher) and Winter Harvest (25% higher) than those reared on cabbage. 5 The intrinsic rate of increase for the G2 of alates of B. brassicae from Chinese cabbage was significantly different on all Brussels sprout cultivars tested. The intrinsic rate of increase differed significantly between aphids reared on either Chinese cabbage or cabbage on cultivars Oliver and Darkmar‐21 (M. persicae) and Red Delicious and Winter Harvest (B. brassicae). The cv. Oliver appeared to be the most consistently good host; Red Delicious was the poorest host overall.

Atmospheric change causes declines in woodland arthropods and impacts specific trophic groups

Arthropod assemblages form a fundamental part of terrestrial ecosystems, underpinning ecosystem processes and services. Yet, little is known about how invertebrate communities, as a whole, respond to climatic and atmospheric changes, including predicted increases in carbon dioxide concentrations (CO2). To date, woodland Free Air CO2 Enrichment (FACE) studies have focused entirely on northern hemisphere managed plantations. We manipulated atmospheric CO2 in a mature, native Eucalyptus woodland (0.15 ha, >32 000 m3) in Australia, using the Eucalyptus FACE (‘EucFACE’) facility. We used three complementary sampling methods (vacuum sampling, pitfall and sticky trapping) to record invertebrate abundances under ambient and elevated levels of CO2 (400 versus 550 ppm). Based on the collection of over 83 000 invertebrates, we found significant declines in the overall abundance of ground‐dwelling (14.7%) and aerial (12.9%) arthropods under elevated CO2, with significant decreases in herbivore, omnivore, scavenger and parasitoid functional groups. Even though several groups showed varying declines in abundance, elevated CO2 did not measurably affect community composition. The results of the present study indicate that atmospheric CO2 levels predicted within the next 35 years may cause declines in arthropod abundances in Eucalyptus woodland. Declines found in several functional groups suggest that elevated atmospheric CO2 has the potential to affect ecosystem processes, possibly including nutrient cycling by herbivores and omnivores, as well as biocontrol by parasitoids.