Root traits with team benefits: understanding belowground interactions in intercropping systems

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Drop when the stakes are high : adaptive, flexible use of dropping behaviour by aphids

RKH was funded by the Perry Foundation and the University of St Andrews. AJK is supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division.For herbivorous insects, dropping from the host plant is a commonly-observed antipredator defence. The use of dropping compared to other behaviours and its timing in relation to contact with a predator was explored in both pea aphids (Acyrthosiphon pisum) and potato aphids (Macrosiphum euphorbiae). Pea aphids dropped more frequently in response to ladybird adults (Adalia bipunctata) than lacewing larvae (Chrysoperla carnea). Potato aphids mainly walked away or backed-up in response to both predator types; but they dropped more frequently relative to other non-walking defences when faced with ladybird adults. Contact with a predator was an important influencer of dropping for both species, and most drops occurred from adjacent to the predator. Dropping appears to be a defence adaptively deployed only when the risk of imminent predation is high; factors that increase dropping likelihood include presence of faster-foraging predators such as adult ladybirds, predator proximity, and contact between aphid and predator.Publisher PDFPeer reviewe

Influence of Hamiltonella defensa infection and predator type on anti-predator behaviours in pea (Acyrthosiphon pisum) and potato aphids (Macrosiphum euphorbiae)

Funding: RKH thanks the Perry Foundation and the University of St Andrews for funding. AJK is supported by the strategic research program funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division.Facultative endosymbionts can induce benefits and costs to their aphid hosts. In the pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae), infection with the γ-proteobacterium Hamiltonella defensa Moran et al. can confer resistance against parasitoids, but may also reduce the frequency of aggressive and escape behaviours exhibited in response to predators. In potato aphids, Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae), H. defensa does not appear to influence susceptibility to parasitism, but its impact on anti-predator behaviours remains unexplored. Here we investigated defensive behaviours in two pea aphid lines (differing in H. defensa-infection status) and four potato aphid lines (that additionally differed in genotype-associated parasitism susceptibility) when faced with foraging ladybirds – Adalia bipunctata (L.) (Coleoptera: Coccinellidae) – and lacewings Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). In response to ladybirds, symbiont-infected pea aphids exhibited proportionately fewer evasive defences (dropping and walking away) than non-infected (cured) pea aphids, but more frequent aggressive kicking. Ladybirds provoked more evasive, aggressive, and total defensive behaviours than lacewings. For potato aphids, symbiont status, predator type, and aphid genotype (i.e., assumed parasitism susceptibility) all influenced behavioural repertoires. Overall, infected lines showed greater differentiation in behaviours in response to the two predators than the uninfected lines. The presence of the symbiont H. defensa may be a key determinant of aphid anti-predator behaviours, but the fitness consequences of this are unresolved. In our study, neither symbiont infection status nor aphid genotype affected the number of aphids consumed by predators.Publisher PDFPeer reviewe

Post-dropping behavior of potato aphids (Macrosiphum euphorbiae)

Funding: Perry Foundation, University of St Andrews, Scottish Government Rural and Environmental Sciences and Analytical Services Division.Dropping behavior is an effective antipredator defense utilized by many insects including aphids, which drop from plants to lower plant parts or underlying substrates to avoid attack from predatory invertebrates. While research commonly focusses on triggers of dropping, less attention is given to what happens to prey individuals following escape drops. In this study, the duration of tonic immobility, recovery rates, and cases of “instant recovery” (re-clinging to lower plant parts) exhibited by potato aphids (Macrosiphum euphorbiae) that dropped from potted seedlings in response to introduced ladybird (Adalia bipunctata) adults, lacewing (Chrysoperla carnea) larvae, and a standardized tactile stimulus were investigated in relation to a range of environmental factors. Air temperature had a negative correlation with the duration of post-dropping tonic immobility; as temperature increased, time spent motionless decreased. Aphids also showed a pattern of increased recovery rate at higher temperatures. Aphids may be selected to move off the substrate quicker to avoid risks of overheating/desiccation at higher temperatures; and/or higher body temperature facilitates locomotion. Stimulus type also influenced recovery rate back to the original seedling, with aphids generally recovering after the standardized stimulus quicker than after dropping triggered by a real predator. Considering cases of instant recovery onto lower-reaches of the host seedling, seedling height influenced the likelihood of re-clinging, with aphids that managed to instantly recover dropping from, on average, taller seedlings than aphids that dropped to the substrate. Plant architecture could mitigate the costs of dropping for aphids, but further studies quantifying understory foliage cover are needed.Publisher PDFPeer reviewe

Limited effects of the maternal rearing environment on the behaviour and fitness of an insect herbivore and its natural enemy

The maternal rearing environment can affect offspring fitness or phenotype indirectly via ‘maternal effects’ and can also influence a mother’s behaviour and fecundity directly. However, it remains uncertain how the effects of the maternal rearing environment cascade through multiple trophic levels, such as in plant-insect herbivore-natural enemy interactions. Pea aphids (Acyrthosiphon pisum) show differential fitness on host legume species, while generalist aphid parasitoids can show variable fitness on different host aphid species, suggesting that maternal effects could operate in a plant-aphid-parasitoid system. We tested whether the maternal rearing environment affected the behaviour and fitness of aphids by rearing aphids on two plant hosts that were either the same as or different from those experienced by the mothers. A similar approach was used to test the behaviour and fitness of parasitoid wasps in response to maternal rearing environment. Here, the host environment was manipulated at the plant or plant and aphid trophic levels for parasitoid wasps. We also quantified the quality of host plants for aphids and host aphids for parasitoid wasps. In choice tests, aphids and parasitoid wasps had no preference for the plant nor plant and aphid host environment on which they were reared. Aphid offspring experienced 50.8% higher intrinsic rates of population growth, 43.4% heavier offspring and lived 14.9% longer when feeding on bean plants compared to aphids feeding on pea plants, with little effect of the maternal rearing environment. Plant tissue nitrogen concentration varied by 21.3% in response to aphid mothers’ rearing environment, and these differences correlated with offspring fitness. Maternal effects in parasitoid wasps were only observed when both the plant and aphid host environment was changed: wasp offspring were heaviest by 10.9–73.5% when both they and their mothers developed in bean-reared pea aphids. Also, parasitoid wasp fecundity was highest by 38.4% when offspring were oviposited in the maternal rearing environment. These findings indicate that maternal effects have a relatively small contribution towards the outcome of plant-aphid-parasitoid interactions

Overcoming barriers to crop diversification uptake in Europe: A mini review

Crop diversification (CD) encompasses practices such as extending crop rotation, cover cropping and intercropping practices, and growing minor crops. It has attracted increasing interest because it can produce both private benefits for farmers, including improved crop and soil health, and reduced inputs, and public goods for society, including greater biodiversity, carbon sequestration, and climate resilience. Nevertheless, CD is not widely practiced in Europe. This paper uses a conceptual framework based upon the literature on barriers to agricultural innovation and CD to guide a systematic-like literature review of existing review articles on the barriers to CD in Europe and a review of research from the European Crop Diversification Cluster, comprising six EU research projects. We compare barriers to CD uptake and identify opportunities to accelerate CD uptake, drawing four main conclusions. First, the barriers to CD are influenced by many factors: the specific crop, cropping method, geographical region, the farmer, the supply chain or market, and the institutional environment. Second, the barriers to CD uptake are interconnected and occur at multiple points along the supply chain; addressing barriers to CD uptake therefore requires a simultaneous and coordinated approach. Third, the inclusion of farmers' perspectives in the CD cluster research revealed novel barriers and solutions demonstrating that participatory and transdisciplinary agricultural research is needed to understand the on-farm reality and its influence on CD uptake. Lastly, farmers' decision-making warrants greater attention. The results highlight that farmers' decision-making is unpredictable and likely to focus on utility rather than profit maximization

Uptake of silicon in barley under contrasting drought regimes

Purpose: Silicon (Si) accumulation in plant tissues plays a vital role in alleviating biotic and abiotic stresses, including drought. Temperate regions are predicted to experience reductions in the quantity and frequency of rainfall events, potentially impacting plant Si uptake via the transpiration stream. Despite the importance for predicting plant responses to Si amendments, the effects of changes in rainfall patterns on Si uptake in cereals have not been characterised. Methods: Five watering regimes were applied based on predicted precipitation scenarios, varying the quantity of water delivered (ambient, 40% or 60% reduction) and watering frequency (40% reduction in quantity, applied 50% or 25% of ambient frequency), and the effects on growth and leaf Si concentrations of a barley landrace and cultivar were determined. Results: Reductions in the quantity of water reduced plant growth and yield, whereas reducing the watering frequency had little impact on growth, and in some cases partially ameliorated the negative effects of drought. Reductions in quantity of water lowered leaf Si concentrations in both the cultivar and landrace, although this effect was alleviated under the drought/deluge watering regime. The landrace had greater leaf Si concentration than the cultivar regardless of watering regime, and under ambient watering deposited Si in all cells between trichomes, whereas the cultivar exhibited gaps in Si deposition. Conclusion: The impact of future reductions in rainfall on barley productivity will depend upon how the water is delivered, with drought/deluge events likely to have smaller effects on yield and on Si uptake than continuous drought

Facilitation and sustainable agriculture: a mechanistic approach to reconciling crop production and conservation

Summary Food security is currently considered a major global problem. However, increasing intensity of food production in agricultural systems has driven reductions in farmland biodiversity. A major challenge is to enable biodiversity conservation whilst addressing the problem of food security. Here we describe how facilitative plant-plant interactions in crop systems could be used to help strike this balance. An obvious example is that of intercropping systems, where combinations of crop species can – under some circumstances – deliver reduced inputs of agrochemicals (fertilisers, pesticides) per unit yield, with potential knock-on benefits for biodiversity conservation. Other facilitative processes can also play a role in biodiversity conservation. Increased intra-specific crop genetic diversity can help protect crops from pests and diseases. Although overlooked in facilitation research, we argue that the mechanisms operate in a manner which is directly analogous to associational defence against herbivores, a process well-recognised in the facilitation literature. As with intercropping, the benefits to nature conservation arise from reduced pesticide use per unit harvested crop. Crops may have facilitative effects on some arable weed species, particularly those that are currently considered rare in intensive farming systems. Work is in its early stages to understand the underlying mechanisms, but it appears that crops might create niche space to which some weed species are adapted. Increasing plant species diversity through niche space creation may then have cascading benefits for other components of farmland biodiversity. Our new understanding of facilitative processes arising from work on crop systems has lessons for the study of facilitative interactions in natural and semi-natural communities. We argue that, although easier to identify and quantify in crop systems, some of these facilitative processes have to date been overlooked in studies of non-crop systems, and certainly deserve further consideration. Finally we discuss what steps may be needed to move from our understanding of the role of facilitation to the development of new agricultural practice. In some cases the challenge may be one of encouraging uptake of existing practices, and in others more research is needed to understand how new ecological understanding might deliver more sustainable agricultural practice

New frontiers in belowground ecology for plant protection from root-feeding insects

Herbivorous insect pests living in the soil represent a significant challenge to food security given their persistence, the acute damage they cause to plants and the difficulties associated with managing their populations. Ecological research effort into rhizosphere interactions has increased dramatically in the last decade and we are beginning to understand, in particular, the ecology of how plants defend themselves against soil-dwelling pests. In this review, we synthesise information about four key ecological mechanisms occurring in the rhizosphere or surrounding soil that confer plant protection against root herbivores. We focus on root tolerance, root resistance via direct physical and chemical defences, particularly via acquisition of silicon-based plant defences, integration of plant mutualists (microbes and entomopathogenic nematodes, EPNs) and the influence of soil history and feedbacks. Their suitability as management tools, current limitations for their application, and the opportunities for development are evaluated. We identify opportunities for synergy between these aspects of rhizosphere ecology, such as mycorrhizal fungi negatively affecting pests at the root-interface but also increasing plant uptake of silicon, which is also known to reduce herbivory. Finally, we set out research priorities for developing potential novel management strategies