Alison J. Karley

Root traits for infertile soils

Crop production is often restricted by the availability of essential mineral elements. For example, the availability of N, P, K, and S limits low-input agriculture, the phytoavailability of Fe, Zn, and Cu limits crop production on alkaline and calcareous soils, and P, Mo, Mg, Ca, and K deficiencies, together with proton, Al and Mn toxicities, limit crop production on acid soils. Since essential mineral elements are acquired by the root system, the development of crop genotypes with root traits increasing their acquisition should increase yields on infertile soils. This paper examines root traits likely to improve the acquisition of these elements and observes that, although the efficient acquisition of a particular element requires a specific set of root traits, suites of traits can be identified that benefit the acquisition of a group of mineral elements. Elements can be divided into three Groups based on common trait requirements. Group 1 comprises N, S, K, B, and P. Group 2 comprises Fe, Zn, Cu, Mn, and Ni. Group 3 contains mineral elements that rarely affect crop production. It is argued that breeding for a limited number of distinct root ideotypes, addressing particular combinations of mineral imbalances, should be pursued.

Downstairs drivers - root herbivores shape communities of above-ground herbivores and natural enemies via changes in plant nutrients

1. Terrestrial food webs are woven from complex interactions, often underpinned by plant-mediated interactions between herbivores and higher trophic groups. Below- and above-ground herbivores can influence one another via induced changes to a shared host plant, potentially shaping the wider community. However, empirical evidence linking laboratory observations to natural field populations has so far been elusive. 2. This study investigated how root-feeding weevils (Otiorhynchus sulcatus) influence different feeding guilds of herbivore (phloem-feeding aphids, Cryptomyzus galeopsidis, and leaf-chewing sawflies, Nematus olfaciens) in both controlled and field conditions. 3. We hypothesized that root herbivore-induced changes in plant nutrients (C, N, P and amino acids) and defensive compounds (phenolics) would underpin the interactions between root and foliar herbivores, and ultimately populations of natural enemies of the foliar herbivores in the field. 4. Weevils increased field populations of aphids by ca. 700%, which was followed by an increase in the abundance of aphid natural enemies. Weevils increased the proportion of foliar essential amino acids, and this change was positively correlated with aphid abundance, which increased by 90% on plants with weevils in controlled experiments. 5. In contrast, sawfly populations were 77% smaller during mid-June and adult emergence delayed by >14 days on plants with weevils. In controlled experiments, weevils impaired sawfly growth by 18%, which correlated with 35% reductions in leaf phosphorus caused by root herbivory, a previously unreported mechanism for above-ground-below-ground herbivore interactions. 6. This represents a clear demonstration of root herbivores affecting foliar herbivore community composition and natural enemy abundance in the field via two distinct plant-mediated nutritional mechanisms. Aphid populations, in particular, were initially driven by bottom-up effects (i.e. plant-mediated effects of root herbivory), but consequent increases in natural enemies triggered top-down regulation.

Raspberry viruses manipulate the behaviour of their insect vectors

Many insect herbivores and plant pathogens influence each other via plant‐mediated mechanisms. Although there is speculation that these interactions may be important in structuring terrestrial food webs, few studies have empirically demonstrated the mechanisms by which pathogens manipulate the behaviour of their insect vectors. We investigated how infection of red raspberry, Rubus idaeus L. (Rosaceae), with two viral pathogens, black raspberry necrosis virus (BRNV) and raspberry leaf mottle virus (RLMV), affected the behaviour of their vector, the large raspberry aphid, Amphorophora idaei Börner (Hemiptera: Aphididae: Macrosiphini). As semi‐persistently transmitted viruses, comparatively little is known about how such viruses affect vector biology. We also examined the effect of infection on plant volatile emissions and amino acid content, which could drive changes in aphid behaviour and performance. Virus‐infected plants were initially more attractive to the aphid and the insects remained on infected plants for 30 min, but were found equally on uninfected plants 12 h after inoculation. Twenty‐seven volatile compounds were identified. Two green leaf volatiles were emitted at higher concentrations by infected plants: (Z)‐3‐hexenyl acetate and 2‐hexenal. In dose‐response assays, (Z)‐3‐hexenyl acetate was attractive to the aphid at concentrations of 50 ng ml−1. When reared on infected plants, aphids took more than 3 days longer to reach adulthood compared with those on uninfected plants, although the number of offspring remained the same. Soluble amino acid (essential and non‐essential) concentrations in raspberry leaves increased more than two‐fold with virus infection. Amino acid composition was dominated by glutamate, accounting for 64 and 77% of the total in uninfected and infected leaves, respectively. Excessive glutamate may have underpinned the negative effects of viral infection on aphid performance. These results demonstrate the capacity of viruses to alter their host plant to manipulate vector behaviour, which may have evolved to be consistent with the transmission requirements of the virus.

Plant Defense against Herbivorous Pests: Exploiting Resistance and Tolerance Traits for Sustainable Crop Protection

Interactions between plants and insect herbivores are important determinants of plant productivity in managed and natural vegetation. In response to attack, plants have evolved a range of defenses to reduce the threat of injury and loss of productivity. Crop losses from damage caused by arthropod pests can exceed 15% annually. Crop domestication and selection for improved yield and quality can alter the defensive capability of the crop, increasing reliance on artificial crop protection. Sustainable agriculture, however, depends on reduced chemical inputs. There is an urgent need, therefore, to identify plant defensive traits for crop improvement. Plant defense can be divided into resistance and tolerance strategies. Plant traits that confer herbivore resistance typically prevent or reduce herbivore damage through expression of traits that deter pests from settling, attaching to surfaces, feeding and reproducing, or that reduce palatability. Plant tolerance of herbivory involves expression of traits that limit the negative impact of herbivore damage on productivity and yield. Identifying the defensive traits expressed by plants to deter herbivores or limit herbivore damage, and understanding the underlying defense mechanisms, is crucial for crop scientists to exploit plant defensive traits in crop breeding. In this review, we assess the traits and mechanisms underpinning herbivore resistance and tolerance, and conclude that physical defense traits, plant vigor and herbivore-induced plant volatiles show considerable utility in pest control, along with mixed species crops. We highlight emerging approaches for accelerating the identification of plant defensive traits and facilitating their deployment to improve the future sustainability of crop protection.

Intraspecific genetic diversity and composition modify species‐level diversity–productivity relationships

Biodiversity regulates ecosystem functions such as productivity, and experimental studies of species mixtures have revealed selection and complementarity effects driving these responses. However, the impacts of intraspecific genotypic diversity in these studies are unknown, despite it forming a substantial part of the biodiversity. In a glasshouse experiment we constructed plant communities with different levels of barley (Hordeum vulgare) genotype and weed species diversity and assessed their relative biodiversity effects through additive partitioning into selection and complementarity effects. Barley genotype diversity had weak positive effects on aboveground biomass through complementarity effects, whereas weed species diversity increased biomass predominantly through selection effects. When combined, increasing genotype diversity of barley tended to dilute the selection effect of weeds. We interpret these different effects of barley genotype and weed species diversity as the consequence of small vs large trait variation associated with intraspecific barley diversity and interspecific weed diversity, respectively. The different effects of intra- vs interspecific diversity highlight the underestimated and overlooked role of genetic diversity for ecosystem functioning.

Plant-mediated effects of drought on aphid population structure and parasitoid attack

The effects of predicted climate change on aphid–natural enemy interactions have principally considered the effects of elevated carbon dioxide concentration and air temperature. However, increased incidence of summer droughts are also predicted in Northern Europe, which could affect aphid–plant interactions and aphid antagonists. We investigated how simulated summer drought affected the bird cherry–oat aphid, Rhopalosiphum padi L., and its natural enemy the parasitoid wasp Aphidius ervi. Drought and, to a greater extent, aphids reduced barley ( Hordeum vulgare) dry mass by 33% and 39%, respectively. Drought reduced leaf and root nitrogen concentrations by 13% and 28%, respectively, but foliar amino acid concentrations and composition remained similar. Aphid numbers were unaffected by drought, but population demography changed significantly; adults constituted 41% of the population on drought‐treated plants, but only 26% on those receiving ambient irrigation. Nymphs constituted 56% and 69% of the population on these plants, respectively, suggesting altered aphid development rates on drought‐stressed plants. Parasitism rates were significantly lower on drought‐stressed plants (9 attacks h−1 compared with 35 attacks h−1 on ambient‐irrigated plants), most likely because of lower incidence of nymphs and more adults, the latter being more difficult to parasitize. Any physiological changes in individual aphids did not affect parasitoid preferences, suggesting that attacks were postponed because of drought‐induced changes in aphid demography. This study demonstrates the potential for sporadic climate change events, such as summer drought, to be disruptive to herbivore–antagonist interactions.

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.

Root symbionts: Powerful drivers of plant above- and belowground indirect defenses

Soil microbial mutualists of plants, including mycorrhizal fungi, non‐mycorrhizal fungi and plant growth promoting rhizobacteria, have been typically characterized for increasing nutrient acquisition and plant growth. More recently, soil microbes have also been shown to increase direct plant defense against above‐ and belowground herbivores. Plants, however, do not only rely on direct defenses when attacked, but they can also recruit pest antagonists such as predators and parasitoids, both above and belowground, mainly via the release of volatile organic compounds (i.e., indirect defenses). In this review, we illustrate the main features and effects of soil microbial mutualists of plants on plant indirect defenses and discuss possible applications within the framework of sustainable crop protection against root‐ and shoot‐feeding arthropod pests. We indicate the main knowledge gaps and the future challenges to be addressed in the study and application of these multifaceted interactions.

Protection of Pea Aphids Associated with Coinfecting Bacterial Symbionts Persists During Superparasitism by a Braconid Wasp

Bacterial endosymbionts that associate facultatively with insect herbivores can influence insect fitness and trophic interactions. The pea aphid, Acyrthosiphon pisum, can be protected from parasitism by the braconid wasp Aphidius ervi when harbouring particular symbiotic bacteria, with specific endosymbiont coinfections providing almost complete protection. However, studies often quantify aphid mummification with no control over parasitoid oviposition per aphid; thus, if mummy production fails or is low, the causes are often unclear. Here, we show that the high level of protection associated with the coinfecting endosymbionts Hamiltonella defensa and X-type is maintained even when pea aphids are superparasitised. This contrasts strongly with the protection provided by H. defensa alone, which has been shown by others to be overcome by superparasitism. By dissecting aphids exposed to two parasitoid attacks, we reveal that A. ervi deposits eggs equally freely in endosymbiont-infected and uninfected nymphs, and lack of mummification in endosymbiont-protected nymphs arises from failure of the wasp eggs to hatch or emerging larvae to develop.

Genotypic variation in the ability of landraces and commercial cereal varieties to avoid manganese deficiency in soils with limited manganese availability: is there a role for root‐exuded phytases?

The marginal agricultural-systems of the Machair in the Western Isles of Scotland often have limited micronutrient availability because of alkaline soils. Traditional landraces of oats, barley and rye are thought to be better adapted to cope with the limited manganese (Mn) availability of these soils. When commercial cultivars are grown on the Machair, limited Mn-availability reduces crop yield and quality. We hypothesised that traditional cereal landraces selected on the Machair acquire Mn more effectively and that this could be linked to exudation of phytase from roots which would release Mn complexed with inositol phosphates. Growth and Mn-acquisition of five landraces and three commercial cultivars of barley and oats were determined in Machair soil. In addition, root phytase activities were assayed under Mn-starvation and sufficiency in hydroponics. In Machair soil, landraces had greater capacity for acquiring Mn and a greater ability to achieve maximum yield compared to the commercial cultivars. Under Mn-starvation, root phytase exudation was upregulated in all plants, suggesting that this trait might allow cereals to acquire more Mn when Mn-availability is limited. In the landraces, exuded phytase activity related positively to relative Mn-accumulation, whereas in the commercial cultivars this relationship was negative, suggesting that this trait may be secondary to an efficiency trait that has been lost from commercial germplasm by breeding. This research shows that cereal landraces possess traits that could be useful for improving the Mn-acquisition of commercial varieties. Exploiting the genetic diversity of landraces could improve the sustainability of agriculture on marginal calcareous lands globally.