James M. W. Ryalls

Effects of elevated temperature and CO2 on aboveground-belowground systems: a case study with plants, their mutualistic bacteria and root/shoot herbivores.

Interactions between above- and belowground herbivores have been prominent in the field of aboveground-belowground ecology from the outset, although little is known about how climate change affects these organisms when they share the same plant. Additionally, the interactive effects of multiple factors associated with climate change such as elevated temperature (eT) and elevated atmospheric carbon dioxide (eCO2) are untested. We investigated how eT and eCO2 affected larval development of the lucerne weevil (Sitona discoideus) and colonization by the pea aphid (Acyrthosiphon pisum), on three cultivars of a common host plant, lucerne (Medicago sativa). Sitona discoideus larvae feed on root nodules housing N2-fixing rhizobial bacteria, allowing us to test the effects of eT and eCO2 across trophic levels. Moreover, we assessed the influence of these factors on plant growth. eT increased plant growth rate initially (6, 8 and 10 weeks after sowing), with cultivar “Sequel” achieving the greatest height. Inoculation with aphids, however, reduced plant growth at week 14. eT severely reduced root nodulation by 43%, whereas eCO2 promoted nodulation by 56%, but only at ambient temperatures. Weevil presence increased net root biomass and nodulation, by 31 and 45%, respectively, showing an overcompensatory plant growth response. Effects of eT and eCO2 on root nodulation were mirrored by weevil larval development; eT and eCO2 reduced and increased larval development, respectively. Contrary to expectations, aphid colonization was unaffected by eT or eCO2, but there was a near-significant 10% reduction in colonization rates on plants with weevils present belowground. The contrasting effects of eT and eCO2 on weevils potentially occurred through changes in root nodulation patterns.

Amino acid-mediated impacts of elevated carbon dioxide and simulated root herbivory on aphids are neutralized by increased air temperatures

Highlight Multiple abiotic factors can combine to alter crop quality and rates of herbivore attack. Aphids benefit from elevated CO2 and root damage, but these effects are neutralized by increased temperatures.

Biology and trophic interactions of lucerne aphids

Lucerne or alfalfa Medicago sativa is the most important temperate forage legume worldwide. Only one or two varieties of lucerne were grown in the U.S.A. and Australia (the two leading exporters of lucerne) before the late 1950s and late 1970s, respectively. These dates coincided with the arrival of aphid species, which devastated lucerne stands and prompted the development of aphid resistant cultivars. Lucerne-feeding aphids, including bluegreen aphids Acyrthosiphon kondoi, pea aphids Acyrthosiphon pisum, spotted alfalfa aphids Therioaphis trifolii maculata and cowpea aphids Aphis craccivora, however, still present significant risks for the lucerne industry worldwide and account for 25% of global production losses. Moreover, increased production costs, negative environmental effects and emerging aphid resistance to insecticide applications have led to a narrowing of management options against lucerne aphids. Understanding lucerne aphid biology and trophic ecology will be needed to develop future management practices, including biological control. We review and synthesize research on the four lucerne aphid species, focussing on cultivar resistance and their interactions with other organisms, including predators, parasitoids, entomopathogens and bacterial symbionts. The effects of global climate change are considered, with a particular emphasis on the potential for compromised aphid resistance in lucerne cultivars under future climates. We conclude by identifying future research questions and perspectives for the sustainable management of lucerne aphids. These include the characterization of plant secondary metabolites associated with natural enemy recruitment, an understanding of the role of endosymbionts in cultivar resistance and a better comprehension of multi-trophic interactions of lucerne aphids, both with other herbivores and higher trophic groups.

The Importance of Testing Multiple Environmental Factors in Legume-Insect Research: Replication, Reviewers, and Rebuttal

Investigating the impacts of predicted changes in our atmosphere and climate change on insect–plant interactions is a widely pursued area of research. To date, the majority of experimental studies have tested the impacts of single environmental factors on insect–plant interactions, but meta-analyses have clearly illustrated the importance of investigating multiple factors in tandem (Zvereva and Kozlov, 2006; Robinson et al., 2012). In particular, environmental change factors often interact with each other which can either strengthen or mitigate the effects of environmental factors acting alone (Robinson et al., 2012). For example, the positive effects of elevated atmospheric carbon dioxide concentrations (e [CO2]) on plant growth are stronger under high nitrogen (N) conditions compared to low N conditions (+ 32 and+ 19%, respectively; Robinson et al., 2012). Likewise, from the limited number of studies available, Robinson et al.(2012) showed that e [CO2] had different impacts on plant nitrogen, plant biomass, and secondary metabolites under elevated air temperature (eT) conditions. This does not invalidate single factor studies, of which we have published numerous examples, but this is an important consideration for making realistic predictions about how plants and insects will respond to future climates (Facey et al., 2014).

Climate and atmospheric change impacts on sap-feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites

Summary 1.Global climate and atmospheric change are widely predicted to affect many ecosystems. Herbivorous insects account for 25% of the planets species so their responses to environmental change are pivotal to how future ecosystems will function. Atmospheric change affects feeding guilds differently, however, with sap-feeding herbivores consistently identified as net beneficiaries of predicted increases in atmospheric carbon dioxide concentrations (eCO2). The mechanistic basis for these effects remains largely unknown and our understanding about how multiple environmental changes, acting in tandem, shape plant–insect interactions is incomplete. 2.This study investigated how increases in temperature (eT) and eCO2 affected the performance of the pea aphid (Acyrthosiphon pisum) via changes in amino acid concentrations in the model legume, lucerne (Medicago sativa). 3.Aphid performance increased under eCO2 at ambient temperatures, whereby aphid fecundity, longevity, colonisation success and rm increased by 42%, 30%, 25% and 21%, respectively. eT negated the positive effects of eCO2 on both fecundity and rm, however, and performance was similar to when aphids were reared at ambient CO2. 4.We identified discrete functional groups of amino acids that underpinned the effects of climate and atmospheric change, in addition to plant genotype, on aphid performance. Effects of eT and eCO2 held true across five M. sativa genotypes, demonstrating the generality of their effects. 5.Combining this knowledge with amino acid profiles of existing cultivars raises the possibility of predicting future susceptibility to aphids and preventing outbreaks of a global pest. Moreover, environmentally-induced changes in the nutritional ecology of aphids have the capacity to change life-history strategies of aphids and their direct and indirect interactions with many other organisms, including mutualists and antagonists. This article is protected by copyright. All rights reserved.

Above–Belowground Herbivore Interactions in Mixed Plant Communities Are Influenced by Altered Precipitation Patterns

Root- and shoot-feeding herbivores have the capacity to influence one another by modifying the chemistry of the shared host plant. This can alter rates of nutrient mineralization and uptake by neighboring plants and influence plant–plant competition, particularly in mixtures combining grasses and legumes. Root herbivory-induced exudation of nitrogen (N) from legume roots, for example, may increase N acquisition by co-occurring grasses, with knock-on effects on grassland community composition. Little is known about how climate change may affect these interactions, but an important and timely question is how will grass–legume mixtures respond in a future with an increasing reliance on legume N mineralization in terrestrial ecosystems. Using a model grass–legume mixture, this study investigated how simultaneous attack on lucerne (Medicago sativa) by belowground weevils (Sitona discoideus) and aboveground aphids (Acyrthosiphon pisum) affected a neighboring grass (Phalaris aquatica) when subjected to drought, ambient, and elevated precipitation. Feeding on rhizobial nodules by weevil larvae enhanced soil water retention under ambient and elevated precipitation, but only when aphids were absent. While drought decreased nodulation and root N content in lucerne, grass root and shoot chemistry were unaffected by changes in precipitation. However, plant communities containing weevils but not aphids showed increased grass height and N concentrations, most likely associated with the transfer of N from weevil-attacked lucerne plants containing more nodules and higher root N concentrations compared with insect-free plants. Drought decreased aphid abundance by 54% but increased total and some specific amino acid concentrations (glycine, lysine, methionine, tyrosine, cysteine, histidine, arginine, aspartate, and glutamate), suggesting that aphid declines were being driven by other facets of drought (e.g., reduced phloem hydraulics). The presence of weevil larvae belowground decreased aphid numbers by 30%, likely associated with a significant reduction in proline in weevil-treated lucerne plants. This study demonstrates how predicted changes to precipitation patterns and indirect interactions between herbivores can alter the outcome of competition between N-fixing legumes and non-N-fixing grasses, with important implications for plant community structure and productivity.

Impacts of silicon-based grass defences across trophic levels under both current and future atmospheric CO2 scenarios

Silicon (Si) has important functional roles in plants, including resistance against herbivores. Environmental change, such as increasing atmospheric concentrations of CO2, may alter allocation to Si defences in grasses, potentially changing the feeding behaviour and performance of herbivores, which may in turn impact on higher trophic groups. Using Si-treated and untreated grasses (Phalaris aquatica) maintained under ambient (400 ppm) and elevated (640 and 800 ppm) CO2 concentrations, we show that Si reduced feeding by crickets (Acheta domesticus), resulting in smaller body mass. This, in turn, reduced predatory behaviour by praying mantids (Tenodera sinensis), which consequently performed worse. Despite elevated CO2 decreasing Si concentrations in P. aquatica, this reduction was not large enough to affect the feeding behaviour of crickets or their predator. Our results suggest that Si-based defences in plants have adverse impacts on both primary and secondary trophic taxa, and these are not likely to decline under future climate change scenarios.

Silicon-induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

Summary Ecologists have become increasingly aware that silicon uptake by plants, especially the Poaceae, can have beneficial effects on both plant growth and herbivore defence. The effects of silicon on other plant functional groups, such as nitrogen-fixing legumes, have been less well studied. Silicon could, however, indirectly promote herbivore performance in this group if reported increases in N2-fixation caused improvements in host plant quality for herbivores. We tested how silicon supplementation in the legume Medico sativa affected plant growth rates, root nodulation and foliage quality (silicon content and amino acid profiles) for an insect herbivore (Acyrthosiphon pisum). Plants supplemented with silicon (Si+) grew three times as quickly as those without supplementation (Si-), almost entirely in shoot mass. While root growth was unaffected by silicon uptake, root nodules containing nitrogen-fixing bacteria were 44% more abundant on Si+ plants. Aphid abundance was twice as high on Si+ plants compared to Si- plants and was positively correlated with silicon-stimulated plant growth. Si+ plants accumulated more than twice as much silicon as Si- plants, but did not have higher silicon concentrations because of dilution effects linked to the rapid growth of Si+ plants. Si+ plants showed a 65% increase in synthesis of essential foliar amino acids, probably due to increased levels of root nodulation. These results suggest that increased silicon supply makes M. sativa more susceptible to A. pisum, mainly because of increased plant growth and resource availability (i.e. essential amino acids). While silicon augmentation of the Poaceae frequently improves herbivore defence, the current study illustrates that this cannot be assumed for other plant families where the beneficial effects of silicon on plant growth and nutrition may promote herbivore performance in some instances. This article is protected by copyright. All rights reserved.

Root responses to domestication, precipitation and silicification: weeping meadow grass simplifies and alters toughness

Background and aimsPlant breeding usually focuses on conspicuous above-ground plant traits, yet roots fundamentally underpin plant fitness. Roots show phenotypic plasticity in response to soil conditions but it is unclear whether domesticated plants respond like their ancestors. We aimed to determine how root traits differed between ancestral and domesticated types of a meadow grass (Microlaena stipoides) under altered regimes of precipitation and soil silicon availability.MethodsWe subjected the two grass types to three simulated precipitation regimes (ambient, +50%/deluge and −50%/drought) in soil with (Si+) and without (Si−) silicon supplementation and then characterised root biomass, architectural complexity and toughness in addition to shoot traits.ResultsDomestication increased root tissue density, decreased specific root length (SRL) and decreased root architectural complexity. Domestication also increased root strength under Si− conditions but not Si+ conditions. Fine roots, SRL, architectural complexity and the force required to tear the roots all decreased under deluge. The ancestral and domesticated grasses responded similarly to precipitation, except that the latter had weaker roots (decreased fracture strain) under drought.ConclusionsDomestication and increased precipitation caused changes in M. stipoides root traits that could be beneficial against some stresses (e.g. soil compaction, herbivory) but not others (e.g. drought).

Belowground Experimental Approaches for Exploring Aboveground–Belowground Patterns

Experiments in aboveground–belowground community ecology are challenging, usually because manipulation and observation of the belowground component is problematic. Problems arise because the soil is an opaque, tri-phasic medium which restricts access and visualisation. While pot studies are commonly used to investigate aboveground–belowground interactions, they have inherent problems including a tendency to cause hypoxic conditions and elevated temperatures. A range of other techniques has been used by ecologists to manipulate belowground factors, in particular. In the laboratory, controlled manipulation includes simulated root damage experiments, split-root experiments and aboveground–belowground olfactometers. Observing belowground components in the laboratory has been achieved using slant boards, rhizotrons, rhizotubes, X-ray tomography and isotope labelling. Manipulation of belowground communities in field experiments either relies on supplementation (e.g. adding organisms) or exclusion (e.g. insecticides), both of which can have confounding effects of experimental manipulations. Observing belowground communities in the field either relies on chemically based and destructive sampling or non-destructive methods (e.g. metal tagging). Researchers continue to innovate with new techniques such as meta-barcoding showing great potential.