Potential contribution of natural enemies to patterns of local adaptation in plants

Genetic differentiation among plant populations and adaptation to local environmental conditions are well documented. However, few studies have examined the potential contribution of plant antagonists, such as insect herbivores and pathogens, to the pattern of local adaptation. Here, a reciprocal transplant experiment was set up at three sites across Europe using two common plant species, Holcus lanatus and Plantago lanceolata. The amount of damage by the main above-ground plant antagonists was measured: a rust fungus infecting Holcus and a specialist beetle feeding on Plantago, both in low-density monoculture plots and in competition with interspecific neighbours. Strong genetic differentiation among provenances in the amount of damage by antagonists in both species was found. Local provenances of Holcus had significantly higher amounts of rust infection than foreign provenances, whereas local provenances of Plantago were significantly less damaged by the specialist beetle than the foreign provenances. The presence of surrounding vegetation affected the amount of damage but had little influence on the ranking of plant provenances. The opposite pattern of population differentiation in resistance to local antagonists in the two species suggests that it will be difficult to predict the consequences of plant translocations for interactions with organisms of higher trophic levels.

The effect of farming system and fertilisers on pests and natural enemies: A synthesis of current research

Organic agriculture is becoming widespread due to increased consumer demand and regulatory and political support. Organic agriculture can increase arthropod diversity but the response of pests and their natural enemies is variable. Fertiliser is an important component of agricultural systems and its effects on pests and natural enemies will influence agroecosystems. In this study, meta-analysis and vote-counting techniques were used to compare farming system (organic and conventional) and fertiliser effects on arthropod pests and their natural enemies. The meta-analyses indicated that pests generally benefitted from organic techniques, this is particularly evident when experiments were carried out on a smaller scale. Pest responses to organic and conventional fertiliser types were divergent, plant composts benefitted pest arthropods while the opposite was true for manures, this has implications for pest management. Most natural enemy groups responded positively to organic farming although this was not true for Coleopterans. Experimental scale had a prominent impact on natural enemy responses with farm scale studies showing particularly positive effects of organic agriculture on natural enemies. This suggests that it is large scale features of organic agriculture such as landscape heterogeneity that are beneficial to natural enemies. Natural enemy responses to organic fertilisers were positive indicating that field scale management practices including fertiliser can also be important in pest management.

The effects of organic and conventional fertilizers on cereal aphids and their natural enemies

Aphids are important pests of spring cereals and their abundance and the impact of their natural enemies may be influenced by fertilizer regime.2We conducted a 2-year field study investigating the effects of organic slow-release and conventional fertilizers on cereal aphids, hymenopteran parasitoids and syrphid predators and considered how the effects of fertilizers on barley morphology and colour might influence these species.3Barley yield was greater in conventionally fertilized pots. Barley morphology was also affected by treatment: vegetative growth was greater under conventional treatments. Barley receiving organic fertilizers or no fertilizer was visually more attractive to aphids compared with plants receiving conventional fertilizers.4Aphids were more abundant in conventionally fertilized barley but the reason for this increased abundance was species specific. Metopolophium dirhodum was responding to fertilizer effects on plant morphology, whereas Rhopalosiphum padi was sensitive to the temporal availability of nutrients.5Syrphid eggs were more numerous in conventionally fertilized pots, whereas the response of parasitoids appeared to be dependent on the abundance of aphids, although the number of parasitoid mummies was low in both years.6This research shows that the fertilizer treatment used can affect numerous characteristics of plant growth and colour, which can then influence higher trophic levels. This knowledge might be used to make more informed fertilizer application choices.

Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops

To manage agroecosystems for multiple ecosystem services, we need to know whether the management of one service has positive, negative, or no effects on other services. We do not yet have data on the interactions between pollination and pest-control services. However, we do have data on the distributions of pollinators and natural enemies in agroecosystems. Therefore, we compared these two groups of ecosystem service providers, to see if the management of farms and agricultural landscapes might have similar effects on the abundance and richness of both. In a meta-analysis, we compared 46 studies that sampled bees, predatory beetles, parasitic wasps, and spiders in fields, orchards, or vineyards of food crops. These studies used the proximity or proportion of non-crop or natural habitats in the landscapes surrounding these crops (a measure of landscape complexity), or the proximity or diversity of non-crop plants in the margins of these crops (a measure of local complexity), to explain the abundance or richness of these beneficial arthropods. Compositional complexity at both landscape and local scales had positive effects on both pollinators and natural enemies, but different effects on different taxa. Effects on bees and spiders were significantly positive, but effects on parasitoids and predatory beetles (mostly Carabidae and Staphylinidae) were inconclusive. Landscape complexity had significantly stronger effects on bees than it did on predatory beetles and significantly stronger effects in non-woody rather than in woody crops. Effects on richness were significantly stronger than effects on abundance, but possibly only for spiders. This abundance-richness difference might be caused by differences between generalists and specialists, or between arthropods that depend on non-crop habitats (ecotone species and dispersers) and those that do not (cultural species). We call this the ‘specialist-generalist’ or ‘cultural difference’ mechanism. If complexity has stronger effects on richness than abundance, it might have stronger effects on the stability than the magnitude of these arthropod-mediated ecosystem services. We conclude that some pollinators and natural enemies seem to have compatible responses to complexity, and it might be possible to manage agroecosystems for the benefit of both. However, too few studies have compared the two, and so we cannot yet conclude that there are no negative interactions between pollinators and natural enemies, and no trade-offs between pollination and pest-control services. Therefore, we suggest a framework for future research to bridge these gaps in our knowledge.

Cereal aphids and their natural enemies: responses to landscape composition and agri-environment schemes

There are potential conflicts between food security, biodiversity conservation and ecosystem services. Currently, there are still gaps in our understanding on the links between land use, biodiversity and ecosystem services; all have implications for sustainable agriculture. To improve food productivity in an ecologically friendly manner we should consider adapting current pest control techniques from being reliant on chemical means towards a more integrated approach. However, to do this, farmers and land owners require more information in order to make informed decisions. This brief review explores field level and landscape scale impacts on aphid control by their natural enemies. This will be done by exploring the effects of local field margin flower strips and two key landscape scale factors, winter wheat and lowland calcareous grasslands on aphids and their natural enemies. Research questions which need answering are discussed.

Foraging strategies of natural enemies of the peach-potato aphid Myzus persicae

The foraging strategies of two natural enemies of the peach-potato aphid Myzus persicae: the seven-spot ladybird Coccinella septempunctata and the parasitoid wasp Diaeretiella rapae, were investigated. Specifically the roles of plant semiochemicals in the location of plants infested with M. persicae by these natural enemies were examined. I investigated the olfactory responses of female C. septempunctata to volatiles collected from M. persicae and four Brassica cultivars; Brassica rapa, B. juncea, B. napus cultivar ‘Apex’ and B. napus cultivar ‘Courage’ and wild-type Arabidopsis thaliana that were: undamaged, previously infested by M. persicae and infested with M. persicae. C. septempunctata showed no attraction to volatiles from M. persicae alone. C. septempunctata significantly changed its searching behaviour in response to plant volatiles from B. rapa, B. napus cv. ‘Apex’ and Arabidopsis infested with M. persicae. C. septempunctata was also found to display a significant turning bias when foraging on a branching horizontal wire stem. A model was developed to investigate how turning biases affect the foraging efficiency of C. septempunctata in dichotomous branched environments. Simulations using this model indicated that turning biases could potentially increase searching efficiency. D. rapae showed a significant preference for volatiles from M. persicae infested wild-type Arabidopsis but no preference to volatiles from M. persicae alone or M. persicae honeydew. Volatile emissions by Arabidopsis were shown to be localised to the area of aphid-infestation rather than systemic. Using gas chromatography plants infested with M. persicae were shown to emit a quantitatively different volatile blend than undamaged plants. In experiments with jasmonate mutants of Arabidopsis the jasmonate (octadecanoid) wound response pathway was implicated as being important for the production of M. persicae induced volatiles, attractive to D. rapae. Other wound response pathways were also found to be involved in the production of the full blend of M. persicae induced volatiles.

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 use of ultraviolet-blocking films in insect pest management in the UK; effects on naturally occurring arthropod pest and natural enemy populations in a protected cucumber crop

Studies in polytunnels were conducted to investigate the effects of ultraviolet (UV)-blocking films on naturally occurring insect pests and their arthropod natural enemies on a cucumber crop. Within tunnels clad with Antibotrytis (blocks light < 400 nm) and UVI/EVA (UV transmitting), 5.8 and 23.4 times more aphids, respectively, were recorded on traps compared with those on traps within tunnels clad with XL 385 (blocks light < 385 nm). When all plants within the UVI/EVA tunnels had become heavily infested with aphids, half of the plants in XL 385 tunnels were uninfested. More Coleoptera and thrips (approximately two times) were recorded under the UVI/EVA film than under the UV-blocking films, but for other arthropod pests (e. g. whitefly, leafhoppers), clear conclusions could not be drawn as low numbers were recorded. Substantial numbers of chalcid parasitoids and syrphids were found under the UV-blocking films, but further research is needed to evaluate fully the effect of such films on biological control of aphids. Higher syrphid numbers and more aphid mummies were recorded under the UVI/EVA film, probably because of the higher numbers of aphids present in tunnels clad with this film. The potential that UV-blocking films have as an effective component of commercial Integrated Pest Management (IPM) systems, for protected horticultural crops, is discussed.

Influence of temperature on pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) resistance to natural enemy attack

The ability to resist or avoid natural enemy attack is a critically important insect life history trait, yet little is understood of how these traits may be affected by temperature. This study investigated how different genotypes of the pea aphid Acyrthosiphon pisum Harris, a pest of leguminous crops, varied in resistance to three different natural enemies (a fungal pathogen, two species of parasitoid wasp and a coccinellid beetle), and whether expression of resistance was influenced by temperature. Substantial clonal variation in resistance to the three natural enemies was found. Temperature influenced the number of aphids succumbing to the fungal pathogen Erynia neoaphidis Remaudiere & Hermebert, with resistance increasing at higher temperatures (18 vs. 28degreesC). A temperature difference of 5degreesC (18 vs. 23degreesC) did not affect the ability of A. pisum to resist attack by the parasitoids Aphidius ervi Haliday and A. eadyi Stary Gonzalez & Hall. Escape behaviour from foraging coccinellid beetles (Hippodamia convergens Guerin-Meneville) was not directly influenced by aphid clone or temperature (16 vs. 21degreesC). However, there were significant interactions between clone and temperature (while most clones did not respond to temperature, one was less likely to escape at 16degreesC), and between aphid clone and ladybird presence (some clones showed greater changes in escape behaviour in response to the presence of foraging coccinellids than others). Therefore, while larger temperature differences may alter interactions between Acyrthosiphon pisum and an entomopathogen, there is little evidence to suggest that smaller changes in temperature will alter pea aphid-natural enemy interactions.

Understanding biodiversity effects on prey in multi-enemy systems

Biodiversity-ecosystem functioning theory would predict that increasing natural enemy richness should enhance prey consumption rate due to functional complementarity of enemy species. However, several studies show that ecological interactions among natural enemies may result in complex effects of enemy diversity on prey consumption. Therefore, the challenge in understanding natural enemy diversity effects is to predict consumption rates of multiple enemies taking into account effects arising from patterns of prey use together with species interactions. Here, we show how complementary and redundant prey use patterns result in additive and saturating effects, respectively, and how ecological interactions such as phenotypic niche shifts, synergy and intraguild predation enlarge the range of outcomes to include null, synergistic and antagonistic effects. This study provides a simple theoretical framework that can be applied to experimental studies to infer the biological mechanisms underlying natural enemy diversity effects on prey.

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.

The effect of acetylsalicylic acid and oxalic acid on Myzus persicae and Aphidius colemani

Plants can respond to damage by pests with both induced direct defences and indirect defences by the attraction of their natural enemies. Foliar application of several plant-derived chemicals, such as salicylic acid and oxalic acid, can induce these defence mechanisms. The effect of acetylsalicylic acid and oxalic acid on the aphid Myzus persicae Sulzer (Homoptera: Aphididae) and its parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae) was investigated. Experiments were carried out with direct application of acetylsalicylic and oxalic acids on these insects, as well as choice and no-choice tests using foliar application of both chemicals on Brussels sprouts plants, Brassica oleracea var. gemmifera L. (Brassicaceae). Parasitoids were given a choice between treated and untreated plants for oviposition, and the effects of the chemicals on aphid and parasitoid development were determined. Although direct application of both chemicals increased aphid mortality, their foliar application did not induce resistance against aphids. The foliar application of such compounds, even in low concentration as shown in the choice tests, has the potential to induce indirect plant defences against aphids by encouraging aphid parasitisation. Although the direct application of both chemicals reduced parasitoid emergence from their hosts, the foliar application of acetylsalicylic acid and low concentrations of oxalic acid did not have a negative effect on parasitoid emergence ability. However, 10 mm oxalic acid reduced the number of emerged parasitoids in no-choice experiments. This study shows that foliar application of acetylsalicylic and oxalic acids has the potential to encourage aphid parasitisation, but care is needed as high concentrations of oxalic acid can have a negative effect on these beneficial organisms.

The population dynamical consequences of density-dependence in fungal plant pathogens

Almost all stages of a plant pathogen life cycle are potentially density dependent. At small scales and short time spans appropriate to a single-pathogen individual, density dependence can be extremely strong, mediated both by simple resource use, changes in the host due to defence reactions and signals between fungal individuals. In most cases, the consequences are a rise in reproductive rate as the pathogen becomes rarer, and consequently stabilisation of the population dynamics; however, at very low density reproduction may become inefficient, either because it is co-operative or because heterothallic fungi do not form sexual spores. The consequence will be historically determined distributions. On a medium scale, appropriate for example to several generations of a host plant, the factors already mentioned remain important but specialist natural enemies may also start to affect the dynamics detectably. This could in theory lead to complex (e.g. chaotic) dynamics, but in practice heterogeneity of habitat and host is likely to smooth the extreme relationships and make for more stable, though still very variable, dynamics. On longer temporal and longer spatial scales evolutionary responses by both host and pathogen are likely to become important, producing patterns which ultimately depend on the strength of interactions at smaller scales.

Aphidius ervi preferentially attacks the green morph of the pea aphid, Acyrthosiphon pisum

The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae) is found in red and green color morphs. Previous work has suggested that the aphidiine parasitoid Aphidius ervi Haliday preferentially attacks green pea aphids in the field. It is not clear whether these results reflect a real preference, or some unknown clonal difference, such as in immunity, between the aphids used in the previous studies. We used three susceptibility-matched pairs of red and green morph pea aphid clones to test for preferences. In a no-choice situation, the parasitoids attacked equal proportions of each color morph. When provided with a choice, A. ervi was significantly more likely to oviposit into colonies formed from green morphs when the neighboring colony was formed from red morph aphids. In contrast, red morphs were less likely to be attacked when their neighboring colony was of the green morph. By preferentially attacking green colonies, A. ervi may reduce the likelihood of intraguild predation, as it is suggested that visually foraging predators preferentially attack red aphid colonies. Furthermore, if this host choice behavior is replicated in the field, we speculate that color morphs of the pea aphid may interact indirectly through their shared natural enemies, leading to intraspecific apparent competition.