Plants in nature have developed many defense mechanisms to defend themselves against attacks by harmful organisms; these mechanisms are indirect and direct. When attacked by a harmful organism, many plant species release volatile substances that attract natural enemies of herbivores. Volatile substances have an important role in the tritrophic system consisting of a plant, a herbivore, and its natural enemy. They function as a kind of chemical signal (semiochemical) which directly influences both harmful pests and their natural enemy. Some of these substances appear on damaged as well as undamaged plants, while other substances are released in the case of mechanic damage or feeding of a particular herbivore species. Volatile substances may repel a herbivore. Harmful pests have an important role in attracting natural enemies, as they also emit chemical signals that function as kairomones for natural enemies. In order to increase our knowledge in the field of indirect plant defense we studied chemosensation of four entomopathogenic nematode species (Steinernema, Heterorhabditis) to compounds released by insect (wireworms and grubs) damaged and undamaged potato and carrot roots, and mechanically damaged maize roots. The aim of our research was (1) to study the effect of different EPN foraging strategies (ambush, intermediate, or cruise) toward the tested volatile compounds, (2) to determine whether chemotaxis is species-specific, and (3) to assess whether the volatile compounds from damaged and undamaged roots have any behavioral effects on the EPNs studied, and (4) if volatile compounds are a part of an indirect plant defense. Our results indicate that all of the tested EPN species exhibited attraction (or repulsion) to volatiles, irrespective of their foraging strategy, and suggest that responses to distinct volatile cues are a species-specific characteristic. These results expand our knowledge of volatile compounds as cues, which may be used by EPNs to find hosts and for other aspects of navigation in soil.
- Volatile compounds
- indirect plant defense
- entomopathogenic nematodes
Plants have a unique role in food chains on the Earth. Like people and animals, plants also contract different diseases caused by fungi, bacteria, viruses, viroids, and phytoplasma . They are also attacked by different animals (insects, mites, nematodes, snails, rodents, game) which feed on them and procreate on them . Each animal species in nature has a unique role and significance. None of them is harmful per se. In natural biotopes we normally do not distinguish between harmful and useful species. This distinction is characteristic for agrarian biotopes, where animals multiply exceedingly and by feeding on cultivated plants causing economic damage . Plant-damaging species are biotic factors which cause economic damage in agriculture and forestry. Useful organisms (biotic agents) are predators, parasitoids, entomopathogenic nematodes (EPNs), entomopathogenic fungi, bacteria, baculoviruses, which suppress harmful pests, and antagonistic microorganisms, which suppress disease agents [3, 4, 5].
Plants in nature have developed many defense mechanisms to defend themselves against attacks by harmful organisms. These mechanisms are indirect and direct [2, 6]. When attacked by a harmful organism, many plant species release volatile substances that attract natural enemies of herbivores [7, 8, 9, 10]. Volatile substances have an important role in the tritrophic system consisting of a plant, a herbivore, and its natural enemy . They function as a kind of chemical signal (semiochemical) which directly influences both harmful pests and their natural enemy [8, 9, 10]. Some of these substances appear on damaged as well as undamaged plants, while other substances are released in the case of mechanic damage or feeding of a particular herbivore species . Volatile substances may repel a herbivore. Harmful pests have an important role in attracting natural enemies, as they also emit chemical signals that function as kairomones for natural enemies .
2. The role of root exudates in rhizosphere
The soil furnishes a living environment to the extremely diverse communities of macro and microorganisms. Likewise, the rhizosphere is the zone of contact in soil surrounding a plant root where biological and chemical parameters of the soil are influenced by the roots. In these niches, complex biological and ecological processes occur . The rhizosphere is a densely populated area in which plant roots must compete with invading root systems of neighboring plants for space, water, and mineral nutrients, and with other soilborne organisms, including insects, bacteria, and fungi . Rhizosphere interactions are based on complex exchanges that evolve around plant roots. Root-based interactions between plants and organisms in the rhizosphere are influenced by edaphic factors . The below-surface biological interactions that are driven by root exudates are more complex than those that occur above the soil surface . These interactions include signal traffic between the roots of competing plants , roots, and soil microbes , and one-way signals that are dependent on the chemical and physical interactions of the soil with the roots .
Unseen part of the plant secretes chemical compounds, which acts as communication signal between the adjacent plant and microbial community present in the rhizosphere of the root. Root exudates correspond to an important source of nutrients for microorganisms in the rhizosphere and seem to participate in early colonization, inducing chemotactic responses of rhizospheric bacteria  and other organisms . Root exudates play an active and relatively well-documented role in the regulation of symbiotic and protective interactions with microbes . Through the exudation of a wide variety of compounds, it is suggested that roots can regulate the soil microbial community in their immediate vicinity, withstand herbivory, encourage beneficial symbioses, change the chemical and physical properties of the soil, and inhibit the growth of competing plant species .
A survey of the literature exposes an extensive range of compounds exuding from intact and healthy roots; these include sugars, amino acids, peptides, enzymes, vitamins, organic acids, nucleotides, fungal stimulators, inhibitors, and attractants . Organic acids, sugars, amino acids, lipids, coumarins, flavonoids, proteins, enzymes, and aliphatic and aromatic compounds are examples of the primary substances found within the rhizosphere in root. Among these substances, the organic acids have received considerable attention due to their role in providing substrates for microbial metabolism and also for serving as intermediates for biogeochemical reactions in soil .
The field of rhizosphere biology has found the relative importance of root exudates in mediating interactions with neighboring plants and microbes . Root exudation is an element of the rhizodeposition process, which is a major source of soil organic carbon released by plant roots . Upon encountering a challenge, roots typically respond by secreting certain small molecules and proteins . Root secretions may play a role in both positive and negative communication in the rhizosphere. The positive communication includes symbiotic associations with beneficial microbes, such as
3. Factors affecting exudation
The exudation of organic compounds by roots are influenced by either biotic (for example, soil microbial uptake)  or abiotic processes . In some instances, our knowledge is sufficient to explain why exudation is affected by the root environment, but often our ignorance of the physiological processes involved in exudation precludes a correct explanation. Some of the factors influencing exudation are listed below.
3.1. Plant species
The amount, range, and balance of compounds in root exudates differ for different plant species.  found differences between wheat and barley (
3.2. Root age
The research performed with peas and oats indicated that more number of amino acids and sugars exude during the first 10 days of growth than those during the second 10 days . Another study  found 3-pyrazolylalanine in root exudate of cucumber (
The release of amino acids, especially asparagine, from roots of tomato and subterranean clover (
Microorganisms may affect the permeability of root cells, metabolism of roots, and absorption and excretion of certain compounds in root exudates. It was reported that filtrates of cultures of some bacteria and fungi and also some antibiotics (penicillin), increased the exudation of scopoletin (6 methoxy -7 hydroxycoumarin) by oat roots . It was found that certain polypeptide antibiotics, for example, polymyxin, produced by
The light intensity at which plants are growing affects the amounts and balance of compounds exuded into nutrient solution by tomato and subterranean clover roots . Clover grown at full daylight intensity exuded more serine, glutamic acid, and c-alanine than plants grown in 60% shade. With tomato, the levels of aspartic acid, glutamic acids, phenylalanine, and leucine in exudate were reduced by shading. Beside these abiotic factors, few others such as moisture, humidity, wind speed and light intensity, elevated CO2 pesticides, available space, atmosphereic nitrogen deposition, ozone, physical disturbance, fire, irrigation, erosion, altitude, and latitude also influence the exudation . Some soil abiotic factors resembling compaction, soil type, salinity, soil pH, metal toxicity, water availability, organic matter, cation and anion exchange, drainage, aeration, rooting depth, soil texture, soil structure, and redox-potential influence the release of organic chemical from plant root .
3.6. Root-feeding insects
Plants in nature are exposed to attacks by insects which bite and suck plants’ parts and thus diminish their vitality. Root-feeding insects play an important role in both agricultural and natural ecosystems . In response to attacks by herbivores, plants excrete terpenes and monoterpenes . So far it has not been established if excretion of volatile substances from damaged plants is due exclusively to attacks by insects or if these substances are stored in plant cells and are excreted only when a plant is in physiological stress . Plants have the so-called morphological defense mechanisms (presence of prickles, thorns, hairs, enzymes, and secondary metabolites), whose presence is not conditioned by attacks of herbivore organisms. Besides morphological defense mechanisms, there are also induced defense mechanisms, which manifest as plants’ reaction to attacks of herbivores. Induced defense mechanisms can be further divided into direct defense mechanisms (secretion of secondary metabolites as a response to attacks by insects) and indirect defense mechanisms (secretion of the [VOCs] VOCs, which attracts natural enemies of herbivore organisms) [6, 42].
Plants react to different types of injuries (mechanical, herbivorous) by excreting different volatile chemical substances, which can be specific also for the insect species attacking a plant . Many studies have shown differences in excretion of volatile compounds from plants which were attacked by different insect species [8, 40, 44]. Simultaneous feeding of different herbivore organisms on a host plant is a very frequent phenomenon in nature , which can influence the success of natural enemies in finding their prey .
VOCs have been commonly identified as arthropod attractants belowground.  highlighted different compounds that are used by herbivores to locate the food source. One of the most important signals in the soils are the emissions of CO2 by roots .  reported that detection of CO2 seems to be dose-dependent, and soil insect are able to detect very small differences in the concentration of CO2. Besides CO2, plants emit various volatile compounds upon herbivore attack. The study of  investigated on-line VOC emissions by roots of
4. The role of root exudates on beneficial soil organisms – Indirect defense against soil herbivores
4.1. Entomopathogenic Nematodes (EPNs)
Tritrophic interactions, which include a host plant, a harmful organism and its natural enemy, have been documented only recently for the underground parts of a plant. Some studies have shown that damaged roots of different plant species release into environment VOCs which can influence the movement of EPNs both as attractans [8, 9, 10, 44] and as repellents .
Soil is the natural habitat of EPNs (Steinernematidae and Heterorhabditidae) (Figure 1), and their application in pest management has been primarily used against soil-inhabiting insect pests . EPNs are lethal pathogens of insects. These pathogens contribute to the regulation of natural populations of insects, but the main interest in them is an inundatively applied biocontrol agent . Their success in this role can be attributed to the unique partnership between a host-seeking nematode and a lethal insect-pathogenic bacterium. Because of their biocontrol potential, considerable attention has been directed over the past few decades to genus,
Although heterorhabditids and steinernematids are not closely related , they share many features in common. These similarities, including their association with insect-pathogenic bacteria, are presumed to have arisen through convergent evolution . In both
The importance of EPNs and biological plant protection against harmful organisms was first established in the USA in the 1930s. In 1923, Glaser and Fox discovered a nematode which attacked and caused death of the beetle,
When EPNs were first discovered, a hypothesis was proposed that nematodes alone cause death of the insects being attacked. In 1937, Bovien first hypothesized the possibility of the existence of symbiotic bacteria that live with EPNs in a mutualistic relationship. His hypothesis was, in 1955, confirmed by Dutky and Weiser . However in 1982, Boemare proved that nematodes from the genus
The use of EPNs in biological plant protection was until some years ago still traditionally connected with suppressing soil-inhabiting insect pests . The research results in the last two decades indicate they have also potential to suppress aboveground insect pests, but only in certain circumstances [71, 72]. Lesser efficiency of EPNs in suppression of aboveground insect pests is primarily due to inappropriate (insufficient) moisture , exposure to thermal extremes , and ultraviolet radiation . These factors are of crucial importance for the survival of nematodes . For this reason nematodes are less efficient against aboveground insect pests outdoors, though the previous laboratory tests showed much higher efficiency .
To lay nematodes on plants, equipments intended for spraying plant protection products, manuring, or irrigation can be used.
IJs can tolerate short-term exposure (2–24 hours) to many chemical and biological insecticides, fungicides, herbicides, fertilizers, and growth regulators and can thus be tank-mixed and applied together [78, 79, 80, 81]. Nematode–chemical combinations in tank-mixes could offer a cost-effective alternative to foliar integrated pest management (IPM) systems.
Due to the sensitivity of nematodes to ultraviolet radiation, nematodes have to be applied to plants in the evening, early in the morning, or during a cloudy weather, when the radiation is not so intense . Nematode survival and efficacy on foliage has also been shown to be enhanced to varying degrees by addition of various adjuvants to the spray mixture, which have antidesiccant (e.g., glycerol, various polymers) or UV-protective (brighteners) properties , although additional measures are required to enhance post-application survival. The greatest potential for using EPNs against foliar pests is almost certain in IPM programs, in conjunction with other biocontrol agents  or selective chemicals [78, 84].
EPNs are considered exceptionally safe biological agents . Because their activity is specific, their environmental risk is considerably lower than that of chemical agents for plant protection . Since the first use of EPNs for suppressing beetles of the species
4.2. Movement of EPNs
The ability of EPN IJs to disperse actively through soil and locate a host is a key element for the successful application of some EPN species in pest management . When an EPN locates its host, it can enter it through natural openings. By excreting its symbiotic bacteria, which release toxins into the host’s body, it causes the death of the insect in 24–72 hours after the infection .
EPNs have through the evolution developed different ways of searching for hosts, which is a species-specific characteristic [89, 90, 91]. The species
EPN species respond distinctly to cues associated with hosts (insects) or plants, depending primarily on their foraging strategy . The cruisers spend most of their time searching for resource-associated cues as they move through their environment [89, 91]. In contrast, ambushers do not respond as strongly as cruisers and spend little time actively moving and searching for volatile cues. Ambushers are thought to wait for resources to come to them [10, 89]. Several EPN species adopt both (cruise and ambush) foraging strategies and are classified as intermediates .
EPNs uses chemosensation to find host, avoid noxious conditions, develop appropriately, and mate. Several authors report that IJs respond to CO2 , temperature, changes in pH, bacterial symbionts , electrical field , and different plant VOCs [8, 9, 10, 44].
4.3. Indirect defense against soil herbivores
Here, we describe our study of the chemotactic behavior of
The results of our research showed that the movement of EPNs was conditioned by the type of VOCs excreted by damaged/undamaged potato tubers (see Figures 2 and 3). VOCs Nonanal, Octanal, and Decanal proved to have a greater influence on the movement of EPNs as other tested volatiles in our investigation. Nonanal and Decanal are among other indicator substances for degradation processes . Decanal is also described to be induced by mechanical and herbivore damage [46, 94, 95].  reports that damaged potato tubers excrete the substances Nonanal, Octanal, and Decanal. The results of our research showed that the said substances acted as attractants in regard to the movement of EPNs. Decanal in our experiment proved as an attractant for the species
In our investigation two distinct VOC concentrations were used. A pure concentration, which does not reflect a concentration found near plant roots , had a bigger influence on IJ movement than a concentration of 0.03 ppm, which is the average concentration of volatile compounds found in soil, 10 cm away from the root system . In our experiment, the difference in responsiveness of EPNs in regard to the concentration of VOC was most substantially expressed in the case of the chemical substance Undecane. At pure concentration, the said substance proved to be an attractant for the species
The results of our research showed that the movement of EPNs toward the selected VOC is substantially determined also by their foraging strategy. In regard to the way of searching the host EPNs fall into three types. Cruisers (
Here, we describe our study of the chemotactic behavior of
Our results show that the chemosensation of IJs toward and away from insect-induced carrot root volatile compounds [50, 100] varied depending on the EPN species, VOC, concentration of VOC, time of exposure and interaction between EPN species and time of exposure (Figures 4 and 5). Our results indicate that all tested EPN species exhibited attraction (or repulsion) to volatiles irrespective of their foraging strategy (in our investigation, terpinolene was a repellent for EPN species classified in all three foraging groups) (Figures 4 and 5). Similar conclusions were also reported in recent research from  in which a cruiser
In our investigation two distinct VOC concentrations were used. A pure concentration, which does not reflect a concentration found near plant roots , had a bigger influence on IJ movement than a concentration of 0.03 ppm, which is the average concentration of VOCs found in soil, 10 cm away from the root system) . However, we are aware that such laboratory studies do not reflect a nematode's true behavior in nature because of exposure to different conflicting chemical signals [44, 101].
Plant roots emit an incredible variety of compounds, which are known to affect interactions between plants and other organisms . The active role plants play in recruiting natural enemies, like belowground herbivores, has been recently demonstrated in a few plant species [8, 10, 88, 96, 102, 103]. EPN host finding is mediated by both long-range cues that facilitate root zone finding, as well as shorter-range cues that facilitate host localization within the root zone [8, 63, 91, 102]. Recently,  reported positive chemotaxis of the two EPN species
Here, we describe our study  of the chemotactic behavior of
The results of our current laboratory investigation showed that the movement and chemosensation of IJs toward and away from damaged maize root VOCs  varied depending on the species, strain, foraging strategy, VOC, and interaction between the EPN strain and volatile compound (see Figure 6). The intermediate foragers (
 reviewed the literature on foraging and host recognition in
Our results suggest that the response to different volatile cues is more a strain-specific characteristic than a different host-searching strategy. Similar conclusions were also made in the research of [9, 91]. Indeed,
The research of VOCs related to plant biotic protection is unequivocally dependent on modern gas chromatography-mass spectrometry (GC-MS), since only this technique allows detection and identification of compounds at such low levels. Due to sample complexity (plant tissue, soil), the use of gas-sampling techniques, which allow sample enrichment, connected with GC-MS, is thus mandatory [8, 12].
The responsiveness of EPNs, the biotic agents which are used for biotic plant protection, was tested in some studies [8, 9, 10, 44]. The studies have shown that damaged plant roots release chemical substances (β-caryophyllene, linalool) which can act as attractants for EPNs. Recently,  reported positive chemotaxis of two EPN species to different VOCs such as heptanol, hexanol, methyl salcylate, etc. Interestingly, they showed that several volatiles repelled the EPNs. Similar effect of VOCs on the behavior of the EPNs was already observed by other researchers [99, 101].
Most VOCs that are involved in belowground tritrophic interactions remain unknown but an increasing effort is being made in this field of research. Understanding more of these complex interactions would not only allow a better understanding of the rhizosphere but could also offer ecologically sound alternatives in pest management of agricultural systems .
Biological control of plants is a way of controlling harmful organisms in agriculture and forestry by making use of live natural enemies (beneficial organisms). It aims to protect and stimulate useful organisms in nature, and to introduce targeted organisms outdoors or into places separated from nature. The application of biotic preparations requires the users to have considerable knowledge and greater ecological awareness. The preparations made biotically are ecologically more appropriate, their functioning is more specific, their formulation and application are important, as is the temporal precision of treatment. Their efficiency, on the other hand, is often lesser than that of chemical preparations, and such preparations are more expensive. The difference in price is due primarily to the relatively small market with biotic agents, which within the entire market of plant protection agents at the moment represent approximately 6% (according to the data of BCC Research), and is expected to rise at least to 8% until 2019.
The value of the global market of biotic agents was in 2013 assessed at approximately 1.8 billion $ and it is expected to reach approximately 4.4 billion $ until 2019. Globally, the USA is still the largest user of biotic agents; it is, however, expected that in the following years the fastest growing market with biotic agents will be Europe, whose strict legislation on plant protection products systematically stimulates ecologic production of food and fodder. Statistical data have shown that the sales of biotic agents between 2005 and 2015 rose by 44%. The expansion of the market is undoubtedly also a consequence of the raised awareness of environmental issues, which are included in the EU directives.
Knowing the communication between plants, herbivores, and their natural enemies is crucial for more efficient implementation and optimization of biological control in food production systems. The European Union has set five ambitious goals – in the fields of employment, innovations, education, social inclusion, and climate/energy – to be reached until 2020. The market with new, improved biotic agents would contribute to environmental protection, as well as to the expansion of economic activities.
This chapter was executed within P4-0013, a program funded by the Slovenian Research Agency. Part of the research presented in this chapter was executed within Professional Tasks from the Field of Plant Protection, which is funded by the Ministry of agriculture, food, and forestry of the Republic of Slovenia – Administration of the Republic of Slovenia for Food Safety, Veterinary Sector, and Plant Protection. Authors are thankful to Jaka Rupnik, Anamarija Jagodič, Anita Klobučar, Neža Ipavec, and Melita Štrukelj for technical assistance.
Solbrig OT. Plant traits and adaptive strategies: their role in ecosystem function. In: Schulze ED, Mooney HA, editors. Biodiversity and Ecosystem Function. Springer Study Edition; 1994. p. 97-116.
Schoonhoven LM., van Loon JJA., Dicke M. Insect-Plant Biology. Oxford: Oxford University Press. 2005. 440 p.
Krieg A, Huger AM, Langenbruch GA, Schnetter W. Bacillus thuringiensisvar tenebrionis: a new pathotype effective against larvae of coleopteran. J Appl Entomol.1983;96:500-508.
Zimmermann G. Review on safety of the entomopathogenic fungi Beauveria bassianaand Beauveria brongniartii. Biocontrol Sci Technol.2007;15:553-596.
Laznik Ž, Trdan S. Entomopathogenic nematodes (Nematoda: Rhabditida) in Slovenia: from tabula rasa to implementation into crop production systems. In: Perveen F, editor. Insecticides – Pest Engineering. Intech, Rijeka, Croatia; 2011.p. 627-656.
Dicke M, Sabelis MW. How plants obtain predatory mites as bodyguards. Neth J Zool1988;38:148-165.
Flores HE, Vivanco JM, Loyola-Vargas VM. ’Radicle’ biochemistry: the biology of root-specific metabolism. Trends Plant Sci.1999;4:220-226.
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature. 2005;434:732-737.
Ali JG, Alborn HT, Stelinski LL. Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatusrecruit entomopathogenic nematodes. J Chem Ecol. 2010;36:361-368.
Laznik Ž, Trdan S. An investigation on the chemotactic responses of different entomopathogenic nematode strains to mechanically damaged maize root volatile compounds. Exp Parasitol. 2013;134:349-355.
Rasmann S, Hiltpold I, Ali J. The role of root-produced volatile secondary metabolites in mediating soil interactions. In: Montanaro G, Cichio B, editors. Advances in Selected Plant Physiology Aspects. InTech Open Access Publisher, Croatia; 2012. p. 269-290.
Weissteiner S, Huetteroth W, Kollmann M, Weißbecker B, Romani R, Schachtner J, Schütz S. Cockchafer larvae smell host root scents in soil. PLoS One. 2012;7:e45827.
Narula N, Kothe E, Behl RK. Role of root exudates in plant-microbe interactions. J Appl Bot Food Qual. 2009;82:122-130.
Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM. How plants communicate using the underground information superhighway. Trends Plant Sci. 2004;9:26-32.
McCully E. Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:695-718.
Yoder JI. Parasitic plant responses to host plant signals: a model for subterranean plant-plant interactions. Curr Opin Plant Biol. 1999;2:65-70.
Wo HH, Kuleck G, Hirsch AM, Hawes MC. Flavonoids: signal molecules in plant development. Adv Exp Med Biol. 2002;505:51-60.
Ryan PR, Delhaize E. Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol. 2001;52:527-560.
Bacilio JM, Aguilar FS, Ventura ZE, Perez CE, Bouquelet S, Zenteno E. Chemical characterization of root exudates from rice ( Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil. 2002;249:271-277.
Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI. Molecular signals and receptors – controlling rhizosphere interactions between plants and other organisms. Ecology. 2003;84:858-868.
Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R, Parvoli G. Soil organic matter mobilization by root exudates. Chemosphere. 2000;4:653-658.
Shukla KP, Sharma S, Singh NK, Singh V, Tiwari K, Singh S. Nature and role of root exudates: Efficacy in bioremediation. Afr J Biotechnol. 2011;10:9717-9724.
Philippe H. Rhizosphere: a new frontier for soil biogeochemistry. J Geol Exp. 2006;88:210-213.
Hutsch BW, Augustin J, Merbach W. Plant rhizodeposition an important source for carbon turnover in soils. J Plant Nut Soil Sci. 2000;165:397-407.
Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell OT. Induced plant defense responses against chewing insects, ethylene signaling reduces resistance of Arabidopsisagainst Egyptian cotton worm but not diamondback moth. Plant Physiol. 2000;124:1007-1018.
Bais HP, Broeckling CD, Vivanco JM. Root exudates modulate plant-microbe interactions in the rhizosphere in secondary metabolites in soil ecology. Soil Biol. 2008;14:241-252.
Kuzyakov Y, Raskatov A, Kaupenjohann M. Turnover and distribution of root exudates of Zea mays. Plant Soil. 2003;254:317-327.
van Hees PAW, Vinogradoff SI, Edwards AC, Godbold DL, Jones DL. Low molecular weight organic acid adsorption in forest soils: effects on soil solution concentrations and biodegradation rates. Soil Biol Biochem. 2003;35:1015-1026.
Vancura V. Root exudates of plants and analysis of root exudates of barley and wheat in their initial phases of growth. Plant Soil. 1964;21:231-248.
Xiaoe YF, Zhenli H, Stoffellab PJ. Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J T Elem Med Biol. 2005;18:339-353.
Rovira AD. Plant root excretions in relation to the rhizosphere effect. I. The nature of root exudate from oats and peas. Plant Soil. 1959;7:178-194.
Vancura V, Hovadik A. Composition of root exudates in the course of plant development. Plant Microb Relat. 1965:21-25.
Hale MG, Moore LD. Factors affecting root exudation. Adv Agron. 1979;31:93-124.
Blaylock MSDE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley B, Raskin E. Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol. 1997;31:860-865.
Norman AG. Microbial products affecting root development. Trans. 7th Congr. Wiscons Int Soil Sci Soc. 1961;2:531-536.
Albert DR. Plant root exudates. Bot Rev. 1969;35:35-57.
Torsvik V, Sorheim R, Goksoyr J. Total bacterial diversity in soil and sediment communities – a review. J Ind Microbiol. 1996;17:170-178.
Rangarajan S, Loganathan P, Saleena M, Nair S. Diversity of Pseudomonasisolated from three di variant plant rhizospheres. J Appl Microbiol. 2001;91:742-749.
Blossey B, Hunt-Joshi TR. Belowground herbivory by insects: Influence on plants and aboveground herbivores. Ann Rev Entomol. 2003;48:521-547.
Takabayashi J, Dicke M. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci. 1996;1:109-113.
Paré PW, Tumlinson JH. Induced synthesis of plant volatiles. Nature. 1997;38:30–31.
Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M. Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol. 2008;19:677-689.
Gosset V, Harmel N, Göbel C, Francis F, Haubruge E, Wathelet JP, du Jardin P, Feussner I, Fauconnier ML. Attacks by piercing-sucking insect ( Myzus persicaeSultzer) or a chewing insect ( Leptinotarsa decemlineataSay) on potato plants ( Solanum tuberosumL.) induce differential changes in volatile compound release and oxylipin synthesis. J Exp Bot. 2009;60:1231-1240.
Hiltpold I, Erb M, Robert CAM, Turlings TCJ. Systemic root signaling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ. 2011;34:1267-1275.
Shiojiri K, Takabayashi J, Yano S, Takafuji A. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul Ecol. 2001;43:23-29.
Dicke M, de Boer JG, Höfte M, Rocha-Granados C. Mixed blends of herbivore- induced plant volatiles and foraging success of carnivorous arthropods. OIKOS. 2003;101:38-48.
Wenke K, Kai M, Piechulla B. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta. 2010;231:499-506.
Johnson SN, Gregory PJ. Chemically-mediated host-plant location and selection by root-feeding insects. Physiol Entomol. 2006;31:1-13.
Crespo E, Hordijk CA, de Graff RM, Samudrala D, Cristescu SM, Harren FJM, van Dam NM. On-line detection of root-induced volatiles in Brassica nigraplants infested with Delia radicumL. root fly larvae. Phytochemistry. 2012;84:68-77.
Weissteiner S. The effect of root volatiles on the orientation behavior of cockchafer larvae in the soil. Dissertation thesis, Georg-August-University-Göttingen. 2010. 182 p.
Sutherland ORW, Hillier JR. Olfactory responses of Costelytra zealandica(Coleoptera: Melolonthinae) larvae to grass root odours. New Zeal J Sci. 1972;15:165-172.
Wolfson JL. Impact of Rhizobium noduleson Sitona hispidulus, the clover root curculio. Entomol Exp Appl. 1987;43:237-243.
Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM, DeMarco SF, Sternberg PW. A sensory code for host seeking in parasitic nematodes. Curr Biol. 2011;21:377-383.
Koppenhöffer AM, Fuzy EM, Crocker R, Gelernter W, Polavarapu S. Pathogenicity of Steinernema scarabaei, Heterorhabditis bacteriophoraand S. glaserito twelve white grub species. Biocontrol Sci Technol. 2004;14:87-92.
Kaya HK, Gaugler R. Entomopathogenic nematodes. Ann Rev Entomol. 1993;38:181-206.
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK. A molecular evolutionary framework for the phylum Nematoda. Nature. 1998;392:71-75.
Poinar GO. Origins and phylogenetic relationships of the entomophilic rhabditids, Heterorhabditisand Steinernema. Fund Appl Nematol. 1993;16:333-338.
Boemare NE, Akhurst RJ, Mourant RG. DNA relatedness between Xenorhabdusspp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescensto a new genus, Photorhabdusgen. Nov. Int J Syst Bacteriol. 1993;43:249-255.
Eidt DC, Thurston GS. Physical deterrents to infection by entomopathogenic nematodes in wireworms (Coleoptera: Elateridae) and other soil insects. Can Entomol. 1995;127:423-429.
Peters A, Ehlers RU. Susceptibility of leather jackets ( Tipula paludosaand Tipula oleracea; Tipulidae: Nematocera) to the entomopathogenic nematode Steinernema feltiae. J Invertebr Pathol. 1994;63:163-171.
Forst S, Clarke D. Bacteria-nematode symbiosis. In: Gaugler R, editor. Entomopathogenic Nematology. Wallingford, UK: CABI Publishing; 2002. p. 57-77.
Kaya HK. Entomopathogenic nematodes and their prospects for biological control in California. In: Hoddle MS, editor. California Conference on Biological Control. Riverside; 2000. p. 38-46.
Hui E, Webster DJ. Influence of insect larvae and seedling roots on the host-finding ability of Steinernema feltiae(Nematoda: Steinernematidae). J Invertebr Pathol. 2000;75:152-162.
Griffin CT, Lewis EE, Boemare N. 'Biology and behaviour'. In: Grewal PS, Ehlers RU, Shapiro-Ilan D, editors. Nematodes as Biocontrol Agents. CABI, Wallingford; 2005. p. 47-64.
Smits PS. Post-application persistence of entomopathogenic nematodes. Biocontrol Sci Technol. 1996;6:379-387.
Glaser RW, Farrell CC. Field experiments with the Japanese beetle and its nematode parasite. J NY Entomol Soc. 1935;43:345.
Gaugler R, Kaya HK. Entomopathogenic Nematodes in Biological Control. Boca Raton, Florida, CRC Press; 1990. 365 p.
Weiser J. Neoaplectana carpocapsaen. sp. (Anguillulata, Steiner-nematidae) novy Cizopasnik housenek obatecejableeneho Carpocapsa pomonellaL. Vestnik Cesk Zool Spoiecnosti. 1955;19:44-52.
Klein MG. Efficacy against soil-inhabiting insect pests. In: Gaugler R, Kaya HK, editors. Entomopathogenic Nematodes in Biological Control. CRC Press, Boca Raton, FL; 1990. p. 195-214.
Ishibashi N, Choi DR. Biological control of soil pests by mixed application of entomopathogenic and fungivorous nematodes. J Nematol. 1991;23:175-181.
Hazir S, Kaya HK, Stock SP, Keskin N. Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turk J Biol. 2004;27:181-202.
Head J, Lawrence AJ, Walters KFA. Efficacy of the entomopathogenic nematode, Steinernema feltiae, against Bemisia tabaciin relation to plant species. J Appl Entomol. 2004;128:543-547.
Lello ER, Patel MN, Mathews GA, Wright DJ. Application technology for entomopathogenic nematodes against foliar pests. Crop Prot. 1996;15:567-574.
Grewal PS, Selvan S, Gaugler R. Thermal adaptation of entomopathogenic nematodes: niche breadth for infection, establishment, and reproduction. J Therm Biol. 1994;19:245-253.
Gaugler R, Bednarek A, Campbell JF. Ultraviolet inactivation of heterorhabditids and steinernematids. J Invertebr Pathol. 1992;59:155-160.
Berry EC, Lewis LC. Interactions between nematodes and earthworms: Enhanced dispersal of Steinernema carpocapsae. J Nematol. 1993;25:189-192.
Wright DJ, Peters A, Schroer S, Fife JP. Application technology. In: Grewal PS, Ehlers RU, Shapiro-Ilan D, editors. Nematodes as Biocontrol Agents. CABI, Wallingford; 2005. p. 91-106.
Head J, Walters KFA, Langton S. The compatibility of the entomopathogenic nematode, Steinernema feltiae, and chemical insecticides for the control of the South American leafminer, Liriomyza huidobrensis. Biocontrol. 2000;45:345-353.
Koppenhöfer AM, Cowles RS, Cowles EA, Fuzy EM, Baumgartner L. Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biol Control. 2002;24:90-97.
Krishnayya PV, Grewal PS. Effect of neem and selected fungicides on viability and virulence of the entomopathogenic nematode Steinernema feltiae. Biocontrol Sci Technol. 2002;12:259-266.
Laznik Ž, Trdan S. The influence of insecticides on the viability of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under laboratory conditions. Pest Manag Sci. 2014;70:784-789.
Grewal PS. Formulation and application technology. In: Gaugler R, editor. Entomopathogenic Nematology. CABI Publishing, CAB International, Wallingford; 2002. p. 311-332.
Sher RB, Parella MP. Biological control of the leafminer, Liriomyza trifolii, in chrysanthemums: implications for intraguild predation between Diglyphus beginiand Steinernema carpocapsae. Bulletin of the International Organization for Biological and Integrated Control of Noxious Animals and Plants: Integrated Control in Glasshouses, 1999;22:221-224.
Rovesti L, Deseo KK. Compatibility of chemical pesticides with entomopathogenic nematodes Steinernema carpocapsaeWeiser and S. feltiaeFilipjev (Nematoda: Steinernematidae). Nematologica. 1990;36:237-245.
Ehlers RU. Mass production of entomopathogenic nematodes for plant protection. Appl Microbiol Biotechnol. 2001;56:623-633.
Ehlers RU. Entomopathogenic nematodes – Save biocontrol agents for sustainable systems. Phytoprotection. 1998;79:94-102.
Akhurst R, Smith K. Regulation and safety. In: Gaugler R, editor. Entomopathogenic Nematology. CABI Publishing, CAB International, Wallingford; 2002. p. 311-332.
Cutler CG, Webster JM. Host-finding ability of three entomopathogenic nematode isolates in the presence of plant roots. Nematology. 2003;5:601-608.
Lewis EE. Behavioural Ecology. In: Gaugler R, editor. Entomopathogenic Nematology. CABI Publishing, CAB International, Wallingford; 2002. p. 205-223.
Campbell JF, Lewis EE, Stock SP, Nadler S, Kaya HK. Evolution of host search strategies in entomopathogenic nematodes. J Nematol. 2003;35:142-145.
Ali JG, Alborn HT, Stelinski LL. Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol. 2011;99:26-35.
Burman M, Pye A. Neoaplectana carpocapsae: movement of nematode populations on thermal gradient. Exp Parasitol. 1980;49:258-265.
Shapiro-Ilan D, Lewis EE, Campbell JF, Kim-Shapiro DB. Directional movement of entomopathogenic nematodes in response to electrical field: effect of species, magnitude of voltage, and infective juvenile age. J Invertebr Pathol. 2012;109:34-40.
Schütz S, Weißbecker B, Klein A, Hummel HE. Host plant selection of the Colorado potatoe beetle as influenced by damage-induced volatiles of the potato plant. Naturwissenschaften. 1997;84:212-217.
Weißbecker B, van Loon JJA, Dicke M. Electroantennogram responses of a predator, Perillus bioculatus, and its prey, Leptinotarsa decemlineata, to plant volatiles. J Chem Ecol. 1999;25:2313-2325.
Köllner TG, Schnee C, Gershenzon J, Degenhardt J. The sesquiterpene hydrocarbons of maize ( Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry. 2004;65:1895-1902.
Grewal PS, Gaugler R, Lewis EE. Host recognition behaviour by entomopathogenic nematodes during contact within insect gut contents. J Parasitol. 1993;79:495-503.
Bell WJ. Searching Behaviour: The Behavioural Ecology of Finding Resources. Chapman & Hall; 1991. 358 p.
Rasmann S, Turlings TCJ. First insights into specificity of belowground tritrophic interactions. Oikos. 2008;117:362-369.
Weissteiner S, Schütz S. Are different volatile pattern influencing host plant choice of belowground living insects? Mitt Dtsch Ges Allg Angew Ent. 2006;15:51-55.
Hiltpold I, Turlings TCJ. Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol. 2008;34:628-635.
van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH. Plants protect their roots by alerting the enemies of grubs. Ecol Lett. 2001;4:292-294.
Neveu N, Grandgirard J, Nenon JP, Cortesero AM. Systematic release of herbivore induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicumL. J Chem Ecol. 2002;28:1717-1732.
Heil M. Indirect defence via tritrophic interactions. New Phytol. 2008;178:41-61.
van Dam NM. Belowground herbivory and plant defenses. Ann Rev Ecol Evol Syst. 2009;40:373-391.
Laznik Ž, Košir IJ, Rozman L, Kač M, Trdan S. Preliminary results of variability in mechanical-induced volatile root-emissions of different maize cultivars. Maydica. 2011;56:343-350.
O’Halloran DM, Burnell AM. An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora. Parasitology. 2003;127:375-385.
Anderson ARA, Young IM, Sleeman BD, Griffiths BS, Robertson WM.. Nematode movement along a chemical gradient in a structurally heterogeneous environment. Experiment Fund Appl Nematol. 1997;20:157-163.
Laznik Ž, Tóth T, Lakatos T, Vidrih M, Trdan S. First record of Steinernema feltiae(Filipjev) (Rhabditida: Steinernematidae) in Slovenia. Helminthologia. 2009;46:135-138.
Stuart RJ, Gaugler R. Genetic adaptation and founder affect in laboratory populations of the entomopathogenic nematode Steinernema glaseri. Can J Zool. 1996;74:164-170.
Nguyen KB, Duncan LW. Steinernema diaprepesi n. sp. (Rhabditida: Steinernematidae), a parasite of the citrus root weevil Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae). J Nematol. 2002;34:159-170.