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Climate Change in the Underworld: Impacts for Soil-Dwelling Invertebrates

2016, Hiltpold, Ivan, Johnson, Scott N., Le Bayon, Renée-Claire, Nielsen, Uffe N.

This chapter reviews and discusses the impact of elevated atmospheric CO2 and climatic changes on three of the functionally most important invertebrate taxa in soil ecosystems: nematodes, insects, and earthworms. The effects of climate and atmospheric CO2 change on soil abiotic conditions vary and numerous biotic feedbacks occur. Many soil‐dwelling insects are herbivores and devastate crops, which impact human societies through yield decreases; therefore an understanding of how climate change will affect their pest status is essential. The chapter discusses potential broader impacts of soil nematode community responses to climate change on ecosystems. Soil‐dwelling insects that feed on roots are usually the juvenile stages of insects that live aboveground as adults. These soil invertebrates can reach astonishing densities, with root‐feeding cicadas of deciduous forests of North America having the largest collective biomass per unit area of any terrestrial animal.

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The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes (Marschner Review for the "Rhizosphere 3" Special Issue)

2012-1-19, Turlings, Ted, Hiltpold, Ivan, Rasmann, Sergio

Background Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO2) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief. Scope This review aims to take away this skepticism by summarizing the evidence for a role of root volatiles as foraging cues for EPNs. To reinforce our argument, we conducted olfactometer assays in which we directly compared the attraction of an EPN species to CO2 and two typical inducible root volatiles. Conclusions The combination of the ubiquitous gas and a more specific root volatile was found to be considerably more attractive than one of the two alone. Hence, future studies on EPN foraging behavior should take into account that CO2 and plant volatiles may work in synergy as attractants for EPNs. Recent research efforts also reveal prospects of exploiting plant-produced signals to improve the biological control of insect pests in the rhizosphere.

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Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm

2012, Hiltpold, Ivan, Hibbard, Bruce Elliott, French, B. W., Turlings, Ted

Aims The use of entomopathogenic nematodes in the biological control of soil insect pests is hampered by the costly and inadequate application techniques. As a possible solution we evaluated a nematode encapsulation approach that offers effective application and may possibly attract the pest by adding attractants to the capsule shell. Methods Heterorhabditis bacteriophora nematodes, which show high virulence against the maize root pest Diabrotica virgifera virgifera, were encapsulated in a polysaccharide shell derived from the algae Laminaria ssp. Shells of varying thickness and composition were evaluated. Results Nematodes readily survived the encapsulation process and were able, varying with shell thickness and temperature, to break through the shell and subsequently infect hosts. The added attractants and feeding stimulants to the shell attracted the pest larvae as much as maize roots. In field trials, encapsulated H. bacteriophora nematodes were more effective in controlling D. v. virgifera than those sprayed in water over the soil surface, but in these trials the addition of stimulants did not increase the control efficiency. Conclusions The study demonstrates that nematodes can be successfully applied in capsules in the field. Further improvements are needed to make the capsules a cost effective alternative to conventional field application of nematodes.

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The Cry of the Corn (Der Hilfeschrei des Mais)

2010, Held, Matthias, D'Alessandro, Marco, Hiltpold, Ivan, Turlings, Ted

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The dual effects of root-cap exudates on nematodes: from quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes

2014, Hiltpold, Ivan, Geoffrey, Jaffuel, Turlings, Ted

To defend themselves against herbivores and pathogens, plants produce numerous secondary metabolites, either constitutively or de novo in response to attacks. An intriguing constitutive example is the exudate produced by certain root-cap cells that can induce a state of reversible quiescence in plant-parasitic nematodes, thereby providing protection against these antagonists. The effect of such root exudates on beneficial entomopathogenic nematodes (EPNs) remains unclear, but could potentially impair their use in pest management programmes. We therefore tested how the exudates secreted by green pea (Pisum sativum) root caps affect four commercial EPN species. The exudates induced reversible quiescence in all EPN species tested. Quiescence levels varied with the green pea cultivars tested. Notably, after storage in root exudate, EPN performance traits were maintained over time, whereas performances of EPNs stored in water rapidly declined. In sharp contrast to high concentrations, lower concentrations of the exudate resulted in a significant increase in EPN activity and infectiousness, but still reduced the activity of two plant-parasitic nematode species. Our study suggests a finely tuned dual bioactivity of the exudate from green pea root caps. Appropriately formulated, it can favour long-term storage of EPNs and boost their infectiousness, while it may also be used to protect plants from plant-parasitic nematodes.

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Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield

2012, Hiltpold, Ivan, Turlings, Ted

In most agro-ecosystems the organisms that feed on plant roots have an important impact on crop yield and can impose tremendous costs to farmers. Similar to aboveground pests, they rely on a broad range of chemical cues to locate their host plant. In their turn, plants have co-evolved a large arsenal of direct and indirect defense to face these attacks. For instance, insect herbivory induces the synthesis and release of specific volatile compounds in plants. These volatiles have been shown to be highly attractive to natural enemies of the herbivores, such as parasitoids, predators, or entomopathogenic nematodes. So far few of the key compounds mediating these so-called tritrophic interactions have been identified and only few genes and biochemical pathways responsible for the production of the emitted volatiles have been elucidated and described. Roots also exude chemicals that directly impact belowground herbivores by altering their behavior or development. Many of these compounds remain unknown, but the identification of, for instance, a key compound that triggers nematode egg hatching to some plant parasitic nematodes has great potential for application in crop protection. These advances in understanding the chemical emissions and their role in ecological signaling open novel ways to manipulate plant exudates in order to enhance their natural defense properties. The potential of this approach is discussed, and we identify several gaps in our knowledge and steps that need to be taken to arrive at ecologically sound strategies for belowground pest management.

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Systemic root signalling in a belowground, volatile-mediated tritrophic interaction

2011, Hiltpold, Ivan, Erb, Matthias, Robert, Christelle Aurélie Maud, Turlings, Ted

Plants attacked by leaf herbivores release volatile organic compounds (VOCs) both locally from the wounded site and systemically from non-attacked tissues. These volatiles serve as attractants for predators and parasitoids. This phenomenon is well described for plant leaves, but systemic induction of VOCs in the roots has remained unstudied. We assessed the spatial and temporal activation of the synthesis and release of (E)-β-caryophyllene (EβC) in maize roots upon feeding by larvae of Diabrotica virgifera virgifera, as well as the importance of systemically produced EβC for the attraction of the entomopathogenic nematode Heterorhabditis megidis. The production of EβC was found to be significantly stronger at the site of attack than in non-attacked tissues. A weak, but significant, increase in transcriptional activity of the EβC synthase gene tps23 and a corresponding increase in EβC content were observed in the roots above the feeding site and in adjacent roots, demonstrating for the first time that herbivory triggers systemic production of a volatile within root systems. In belowground olfactometers, the nematodes were significantly more attracted towards local feeding sites than systemically induced roots. The possible advantages and disadvantages of systemic volatile signalling in roots are discussed.

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Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field

2013, Robert, Christelle Aurélie Maud, Erb, Matthias, Hiltpold, Ivan, Hibbard, Bruce Elliott, Gaillard, Mickaël David Philippe, Bilat, Julia, Degenhardt, Jörg, Cambet-Petit-Jean, Xavier, Turlings, Ted, Zwahlen, Claudia

Genetic manipulation of plant volatile emissions is a promising tool to enhance plant defences against herbivores. However, the potential costs associated with the manipulation of specific volatile synthase genes are unknown. Therefore, we investigated the physiological and ecological effects of transforming a maize line with a terpene synthase gene in field and laboratory assays, both above- and below ground. The transformation, which resulted in the constitutive emission of (E)--caryophyllene and -humulene, was found to compromise seed germination, plant growth and yield. These physiological costs provide a possible explanation for the inducibility of an (E)--caryophyllene-synthase gene in wild and cultivated maize. The overexpression of the terpene synthase gene did not impair plant resistance nor volatile emission. However, constitutive terpenoid emission increased plant apparency to herbivores, including adults and larvae of the above ground pest Spodoptera frugiperda, resulting in an increase in leaf damage. Although terpenoid overproducing lines were also attractive to the specialist root herbivore Diabrotica virgifera virgifera below ground, they did not suffer more root damage in the field, possibly because of the enhanced attraction of entomopathogenic nematodes. Furthermore, fewer adults of the root herbivore Diabrotica undecimpunctata howardii were found to emerge near plants that emitted (E)--caryophyllene and -humulene. Yet, overall, under the given field conditions, the costs of constitutive volatile production overshadowed its benefits. This study highlights the need for a thorough assessment of the physiological and ecological consequences of genetically engineering plant signals in the field to determine the potential of this approach for sustainable pest management strategies.

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The Role of Root-Produced Volatile Secondary Metabolites in Mediating Soil Interactions

2012, Rasmann, Sergio, Hiltpold, Ivan, Ali, Jared G, Montanaro, Giuseppe, Dichio, Bartolomeo

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The role of volatile organic compounds in the indirect defense of plants against insect herbivores above- and belowground

2010, Held, Matthias, D'Alessandro, Marco, Hiltpold, Ivan, Turlings, Ted