Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid

The role of indirect interactions in structuring communities is becoming increasingly recognised. Plant fungi can bring about changes in plant chemistry which may affect insect herbivores that share the same plant, and hence the two may interact indirectly. This study investigated the indirect effects of a fungal pathogen (Marssonina betulae) of silver birch (Betula pendula) on an aphid (Euceraphis betulae), and the processes underpinning the interaction. There was a strong positive association between natural populations of the aphid and leaves bearing high fungal infection. In choice tests, significantly more aphids settled on leaves inoculated with the fungus than on asymptomatic leaves. Individual aphids reared on inoculated leaves were heavier, possessed longer hind tibiae and displayed enhanced embryo development compared with aphids reared on asymptomatic leaves; population growth rate was also positively correlated with fungal infection when groups of aphids were reared on inoculated branches. Changes in leaf chemistry were associated with fungal infection with inoculated leaves containing higher concentrations of free-amino acids. This may reflect a plant-initiated response to fungal attack in which free amino acids from the degradation of mesophyll cells are translocated out of infected leaves via the phloem. These changes in plant chemistry are similar to those occurring during leaf senescence, and are proposed as the mechanistic basis for the positive interaction between the fungus and aphid.

Phytohormones and plant-herbivore-pathogen interactions: integrating the molecular with the ecological

Current research into indirect phytopathogen–herbivore interactions (i.e., interactions mediated by the host plant) is carried out in two largely independent directions: ecological/mechanistic and molecular. We investigate the origin of these approaches and their strengths and weaknesses. Ecological studies have determined the effect of herbivores and phytopathogens on their host plants and are often correlative: the need for long-term manipulative experiments is pressing. Molecular/cellular studies have concentrated on the role of signaling pathways for systemic induced resistance, mainly involving salicylic acid and jasmonic acid, and more recently the cross-talk between these pathways. This cross-talk demonstrates how interactions between signaling mechanisms and phytohormones could mediate plant–herbivore–pathogen interactions. A bridge between these approaches may be provided by field studies using chemical induction of defense, or investigating whole-organism mechanisms of interactions among the three species. To determine the role of phytohormones in induced resistance in the field, researchers must combine ecological and molecular methods. We discuss how these methods can be integrated and present the concept of “kaleidoscopic defense.” Our recent molecular-level investigations of interactions between the herbivore Gastrophysa viridula and the rust fungus Uromyces rumicis on Rumex obtusifolius, which were well studied at the mechanistic and ecological levels, illustrate the difficulty in combining these different approaches. We suggest that the choice of the right study system (possibly wild relatives of model species) is important, and that molecular studies must consider the environmental conditions under which experiments are performed. The generalization of molecular predictions to ecologically realistic settings will be facilitated by “middle-ground studies” concentrating on the outcomes of the interactions.

Influence of host plant heterogeneity on the distribution of a birch aphid

1. The spatial and temporal abundance of the aphid Euceraphis betulae was investigated in relation to heterogeneity in host plant ( Betula pendula) vigour and pathogenic stress. The performance of aphids feeding on vigorous and stressed foliage was also examined. 2. The plant stress and plant vigour hypotheses have been suggested as opposing ways in which foliage quality influences herbivore abundance. In many plants, however, vigorous growing foliage co-exists with stressed or damaged foliage. 3. There was a negative correlation between branch growth ( vigour) and branch stress ( leaf chlorosis), with the most vigorous branches displaying little or no stress, and the most stressed branches achieving poor growth. There was a similar negative correlation between vigour and stress at the level of individual trees, which themselves represented a continuum in quality. 4. At the beginning of the season, E. betulae were intermittently more abundant on vigorous branches than on branches destined to become stressed, but aphids became significantly more abundant on stressed branches later in the season, when symptoms of stress became apparent. Similar patterns of aphid abundance were seen on vigorous and stressed trees in the following year. 5. Euceraphis betulae performance was generally enhanced when feeding on naturally stressed B. pendula leaves, but there was some evidence for elevated potential reproduction when feeding on vigorous leaves too. 6. Overall, plant stress probably influences E. betulae distribution more than plant vigour, but the temporal and spatial variability in plant quality suggests that plant vigour could play a role in aphid distribution early in the season.

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.

Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis

1. The growth (increase in height and leaf number) of four grass species was reduced by a -0.5 MPa drought stress, but the performance of an associated herbivore, Rhopalosiphum padi (L.), was not affected consistently. The intrinsic rate of increase of R. padi was reduced by drought stress on three grass species, including Dactylis glomerata (L.), but was unaffected on Arrhenatherum elatius (L.). Therefore, there is no general relationship in the effect of plant drought on an insect herbivore, even among closely related host plant species. 2. Drought stress increased the quality of plant phloem sap, as indicated by increased sieve element osmotic pressure and essential amino acid concentrations. Thus, diet quality could not account for the reduced performance of R. padi under drought stress. The concentration of essential amino acids in the phloem of well-watered A. elatius was, however, lower than that of well-watered D. glomerata, correlating with the decreased performance of aphids on well-watered A. elatius. 3. There were no differences in aphid feeding duration between watering treatments or plant species but sap ingestion rates were reduced significantly under drought stress. 4. Using the measure of dietary amino acid concentrations and the estimate of sap ingestion, the essential amino acid flux through aphids was calculated. Compared with the flux through aphids feeding on well-watered D. glomerata, there was a reduction in aphids feeding on drought-stressed D. glomerata and drought-stressed A. elatius due to lower sap ingestion rates. The flux through aphids on well-watered A. elatius was also reduced due to low phloem essential amino acid concentrations. Thus, the performance of an aphid is correlated with the availability and accessibility of essential amino acids.

Effects of summer rainfall manipulations on the abundance and vertical distribution of herbivorous soil macro-invertebrates

Soil invertebrate communities are likely to be highly vulnerable to low soil moisture, caused by a reduction in summer rainfall which is predicted for some regions under current climate change scenarios. However, the effects of changes in summer rainfall on soil invertebrate assemblages have rarely been tested experimentally. In this study, samples were taken in 2003 and 2004 from a long-running field experiment, to investigate the impact of 10 years of experimental summer drought and increased summer rainfall manipulations on the soil fauna of a calcareous grassland. Summer drought altered the soil invertebrate assemblage in the autumn, immediately following treatment application, but by the following spring treatment effects were no longer apparent. The two most common root herbivore species responded differently to the summer rainfall manipulations. Larvae of the dominant root-chewing species, Agriotes lineatus, were more numerous under enhanced rainfall in both the spring and autumn. In contrast, abundance of the Coccoidea Lecanopsis formicarum was unaffected by the rainfall manipulations. The responses of root herbivores to an increased incidence of summer droughts are therefore likely to vary, depending on their feeding strategy and life history. (c) 2007 Elsevier Masson SAS. All rights reserved.

Drought impacts on above-belowground interactions: do effects differ between annual and perennial host species?

Root herbivores can have a positive or negative effect on the abundance and/or performance of foliar phytophages. In addition, abiotic factors such as drought can either strengthen or weaken this effect, depending on the system under investigation. One explanation for these varying responses lies in differences in the physiological response of host plants to drought and root herbivores. Here, the impacts of root phytophages on a leaf-mining species feeding on annual and perennial plant species (four Sonchus species) were compared. The responses of plants and leaf-miners to dtought and root herbivore treatments were not related to whether the host plant was an annual or perennial. However, where root feeders did affect foliar phytophage performance, this occurred only under a drought treatment, demonstrating the potential for climatic change to alter the outcome of plant-mediated interactions. (c) 2007 Gessellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Host niches and defensive extended phenotypes structure parasitoid wasp communities

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies. Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the "Enemy Hypothesis,'' which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.

Intra-specific variation affects the structure of the natural enemy assemblage attacking pea aphid colonies

1. Intra-specific variation in plant defence traits has been shown to profoundly affect herbivore community structure. Here we describe two experiments designed to test whether similar effects occur at higher trophic levels, by studying pea aphid–natural enemy interactions in a disused pasture in southern England. 2. In the first experiment, the numbers and identity of natural enemies attacking different monoclonal pea aphid colonies were recorded in a series of assays throughout the period of pea aphid activity. 3. In the summer assay, there was a significant effect of clone on the numbers of aphidophagous hoverfly larvae and the total number of non-hoverfly natural enemies recruited. Clone also appeared to influence the attack rate suffered by the primary predator in the system, the hoverfly Episyrphus balteatus, by Diplazon laetatorius, an ichneumonid parasitoid. Colonies were generally driven to extinction by hoverfly attack, resulting in the recording of low numbers of parasitoids and entomopathogens, suggesting intense intra-guild predation. 4. To further examine the influence of clonal variation on the recruitment of natural enemies, a second experiment was performed to monitor the temporal dynamics of community development. Colonies were destructively sampled every other day and the numbers of natural enemies attacking aphid colonies were recorded. These data demonstrated that clonal variation influenced the timing, abundance, and identity of natural enemies attacking aphid colonies. 5. Taken together, these data suggest that clonal variation may have a significant influence on the patterns of interactions between aphids and their natural enemies, and that such effects are likely to affect our understanding of the ecology and biological control of these insect herbivores.

The role of exotic plants in the invasion of Seychelles by the polyphagous insect Aleurodicus disperses: a phylogenetically controlled analysis

The accidental introduction of the spiralling whitefly, Aleurodicus dispersus Russell (Homoptera: Aleyrodidae) to Seychelles in late 2003 is exploited during early 2005 to study interactions between A. dispersus, native and exotic host plants and their associated arthropod fauna. The numbers of A. dispersus egg spirals and pupae, predator and herbivore taxa were recorded for eight related native/exotic pairs of host plants found on Mahe, the largest island in Seychelles. Our data revealed no significant difference in herbivore density (excluding A. dispersus) between related native and exotic plants, which suggests that the exotic plants do not benefit from 'enemy release'. There were also no differences in predator density, or combined species richness between native and exotic plants. Together these data suggest that 'biotic resistance' to invasion is also unlikely. Despite the apparent lack of differences in community structure significantly fewer A. dispersus egg spirals and pupae were found on the native plants than on the exotic plants. Additional data on A. dispersus density were collected on Cousin Island, a managed nature reserve in which exotic plants are carefully controlled. Significantly higher densities of A. dispersus were observed on Mahe, where exotic plants are abundant, than on Cousin. These data suggest that the rapid invasion of Seychelles by A. dispersus may largely be due to the high proportion of plant species that are both exotic and hosts of A. dispersus; no support was found for either the 'enemy release' or the 'biotic resistance' hypotheses.

Suitability of Arabidopsis thaliana as a model for host plant-Plutella xylostella-Cotesia plutellae interactions

Successful pest management is often hindered by the inherent complexity of the interactions of a pest with its environment. The use of genetically characterized model plants can allow investigation of chosen aspects of these interactions by limiting the number of variables during experimentation. However, it is important to study the generic nature of these model systems if the data generated are to be assessed in a wider context, for instance, with those systems of commercial significance. This study assesses the suitability of Arabidopsis thaliana (L.) Heynh. (Brassicaceae) as a model host plant to investigate plant-herbivore-natural enemy interactions, with Plutella xylostella (L.) (Lepidoptera: Plutellidae), the diamondback moth, and Cotesia plutellae (Kurdjumov) (Hymenoptera: Braconidae), a parasitoid of P. xylostella. The growth and development of P. xylostella and C. plutellae on an A. thaliana host plant (Columbia type) were compared to that on Brassica rapa var. pekinensis (L.) (Brassicaceae), a host crop that is widely cultivated and also commonly used as a laboratory host for P. xylostella rearing. The second part of the study investigated the potential effect of the different A. thaliana background lines, Columbia and Landsberg (used in wider scientific studies), on growth and development of P. xylostella and C. plutellae. Plutella xylostella life history parameters were found generally to be similar between the host plants investigated. However, C. plutellae were more affected by the differences in host plant. Fewer adult parasitoids resulted from development on A. thaliana compared to B. rapa, and those that did emerge were significantly smaller. Adult male C. plutellae developing on Columbia were also significantly smaller than those on Landsberg A. thaliana.

Relative importance of fertiliser addition to plants and exclusion of predators for aphid growth in the field

Herbivore dynamics and community structure are influenced both by plant quality and the actions of natural enemies. A factorial experiment manipulating both higher and lower trophic levels was designed to explore the determinants of colony growth of the aphid Aphis jacobaeae, a specialist herbivore on ragwort Senecio jacobaea. Potential plant quality was manipulated by regular addition of NPK-fertiliser and predator pressure was reduced by interception traps; the experiment was carried out at two sites. The size and persistence of aphid colonies were measured. Fertiliser addition affected plant growth in only one site, but never had a measurable effect on aphid colony growth. In both habitats the action of insect predators dominated, imposing strong and negative effects on aphid colony performance. Ants were left unmanipulated in both sites and their performance on the aphid colonies did not significantly differ between sites or between treatments. Our results suggest that, at least for aphid herbivores on S. jacobaea, the action of generalist insect predators appears to be the dominant factor affecting colony performance and can under certain conditions even improve plant productivity.

Chemistry and biology of maculalactone A from the marine cyanobacterium Kyrtuthrix maculans

Maculalactone A is the most abundant secondary metabolite in Kyrtuthrix maculans, a marine cyanobacterium found in the mid-high shore of moderately exposed to sheltered rocky shores in Hong Kong and South East Asia. This species appears to survive as pure colonies forming distinct black zones on the rock. Maculalactone A may provide K. maculans with a chemical defense against several marine organisms, including the common grazer, Chlorostoma argyrostoma and settlement by larvae of the barnacles, Tetraclita japonica, Balanus amphitrite and Ibla cumingii. The natural concentration of maculalactone A varied with season and also with tidal height on the shore and although a strong positive linear correlation was observed between maculalactone A concentration and herbivore grazing pressure, manipulative experiments demonstrated that grazing pressure was not directly responsible for inducing the biosynthesis of this metabolite. The potential of maculalactone A as a natural marine anti-fouling agent (i.e. as an alternative to environmentally-damaging copper- and tin-based anti-fouling paints) was investigated after achieving a gram-scale synthesis of this compound. Preliminary field trials with anti-fouling paints which contained synthetic maculalactone A as the active principle have confirmed that this compound seems to have a specific activity against molluscan settlers.

Limiting factors in the restoration of UK grassland beetle assemblages

Grasslands restoration is a key management tool contributing to the long-term maintenance of insect populations, providing functional connectivity and mitigating against extinction debt across landscapes. As knowledge of grassland insect communities is limited, the lag between the initiation of restoration and the ability of these new habitats to contribute to such processes is unclear. Using ten data sets, ranging from 3 to 14 years, we investigate the lag between restoration and the establishment of phytophagous beetle assemblages typical of species rich grasslands. We used traits and ecological characteristics to determine factors limiting beetle colonisation, and also considered how food-web structure changed during restoration. For sites where seed addition of host-plants occurred the success in replicating beetle assemblages increased over time following a negative exponential function. Extrapolation beyond the existing data set tentatively suggested that success would plateau after 20 years, representing a c. 60% increase in assemblage similarity to target grasslands. In the absence of seed addition, similarity to the target grasslands showed no increase over time. Where seed addition was used the connectance of plant-herbivore food webs decreased over time, approaching values typical of species rich grasslands after c. 7 years. This trend was, however, dependent on the inclusion of a single site containing data in excess of 6 years of restoration management. Beetles not capable of flight, those showing high degrees of host-plant specialisation and species feeding on nationally rare host plants take between 1 and 3 years longer to colonise. Successful grassland restoration is underpinned by the establishment of host-plants, although individual species traits compound the effects of poor host-plant establishment to slow colonisation. The use of pro-active grassland restoration to mitigate against future environmental change should account for lag periods in excess of 10 years if the value of these habitats is to be fully realised.

Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites

Predicting how insect crop pests will respond to global climate change is an important part of increasing crop production for future food security, and will increasingly rely on empirically based evidence. The effects of atmospheric composition, especially elevated carbon dioxide (eCO(2)), on insect herbivores have been well studied, but this research has focussed almost exclusively on aboveground insects. However, responses of root-feeding insects to eCO(2) are unlikely to mirror these trends because of fundamental differences between aboveground and belowground habitats. Moreover, changes in secondary metabolites and defensive responses to insect attack under eCO(2) conditions are largely unexplored for root herbivore interactions. This study investigated how eCO(2) (700 mu mol mol-1) affected a root-feeding herbivore via changes to plant growth and concentrations of carbon (C), nitrogen (N) and phenolics. This study used the root-feeding vine weevil, Otiorhynchus sulcatus and the perennial crop, Ribes nigrum. Weevil populations decreased by 33% and body mass decreased by 23% (from 7.2 to 5.4 mg) in eCO(2). Root biomass decreased by 16% in eCO(2), which was strongly correlated with weevil performance. While root N concentrations fell by 8%, there were no significant effects of eCO(2) on root C and N concentrations. Weevils caused a sink in plants, resulting in 8-12% decreases in leaf C concentration following herbivory. There was an interactive effect of CO(2) and root herbivory on root phenolic concentrations, whereby weevils induced an increase at ambient CO(2), suggestive of defensive response, but caused a decrease under eCO(2). Contrary to predictions, there was a positive relationship between root phenolics and weevil performance. We conclude that impaired root-growth underpinned the negative effects of eCO(2) on vine weevils and speculate that the plant's failure to mount a defensive response at eCO(2) may have intensified these negative effects.