Plant Protect. Sci., 2019, 55(4):243-254 | DOI: 10.17221/24/2019-PPS

Entomopathogenic nematodes: can we use the current knowledge on belowground multitrophic interactions in future plant protection programmes? - ReviewReview

Anamarija Jagodiè, Stanislav Trdan, ®iga Laznik*
Department of Agronomy, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

Plants under herbivore attack emit mixtures of volatiles that can attract the natural enemies of the herbivores. Entomopathogenic nematodes (EPNs) are organisms that can be used in the biological control of insect pests. Recent studies have shown that the movement of EPNs is associated with the detection of chemical stimuli from the environment. To date, several compounds that are responsible for the mediation in below ground multitrophic interactions have been identified. In the review, we discuss the use of EPNs in agriculture, the role of belowground volatiles and their use in plant protection programmes.

Keywords: insects; indirect plant defence; volatile organic compounds; chemical communication; insect parasitic nematodes

Published: December 31, 2019  Show citation

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Jagodiè A, Trdan S, Laznik ®. Entomopathogenic nematodes: can we use the current knowledge on belowground multitrophic interactions in future plant protection programmes? - Review. Plant Protect. Sci. 2019;55(4):243-254. doi: 10.17221/24/2019-PPS.
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    References

    1. Akhurst R., Smith K. (2002): Regulation and safety. In: Gaugler R. (ed.): Entomopathogenic Nematology. Wallingford, CABI Publishing: 311-332. Go to original source...
    2. Ali J.G., Alborn H.T., Stelinski L.L. (2010): Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. Journal of Chemical Ecology, 36: 361-368. Go to original source... Go to PubMed...
    3. Ali J.G., Alborn H.T., Stelinski L.L. (2011): Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. Journal of Ecology, 99: 26-35. Go to original source...
    4. Alleyne M., Beckage N.E. (1997): Parasitism-induced effects on host growth and metabolic efficiency in tobacco hornworm larvae parasitised by Cotesia congregata. Journal of Insect Physiology, 43: 407-424. Go to original source... Go to PubMed...
    5. Bais H.P., Weir T.L., Perry L.G., Gilroy S., Vivanco J.M. (2006): The role of root exudates in rhizosphere interations with plants and other organisms. Annual Review of Plant Biology, 57: 233-266. Go to original source... Go to PubMed...
    6. Benrey B., Callejas A., Rios L., Oyama K., Denno R.F. (1998): The effects of domestification of Brassica and Phaseolus on the interaction between phytophagus insects and parasitiods. Biological Control, 11: 130-140. Go to original source...
    7. Boemare N.E., Laumond C., Luciani J. (1982): Mise en évidence d'une toxicogénèse provoquée par le nématode axénique entomophage Neoplectana carpocapsae, Weiser chez l'insecte Galleria mellonella L. Comptes rendus des séances de l'Academie des Sciences, 295: 543-546.
    8. Boff M.I.C., Zoon F.C., Smits P.H. (2001): Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomologia Experimentalis et Applicata, 98: 329-337. Go to original source...
    9. Braasch J., Kaplan I. (2012): Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage. Entomologia Experimentalis et Applicata, 145: 115-123. Go to original source...
    10. Brillada C., Nishihara M., Shimoda T., Garms S., Boland W., Maffei M.E., Arimura G.I. (2013): Metabolic engineering of the C 16 homoterpene TMTT in Lotus japonicus through overexpression of (E,E)-geranyllinalool synthase attracts generalist and specialist predators in different manners. New Phytologist Trust, 200: 1200-1211. Go to original source... Go to PubMed...
    11. Burman M., Pye A. (1980): Neoaplectana carpocapsae: movement of nematode populations on thermal gradient. Experimental Parasitology, 49: 258-265. Go to original source... Go to PubMed...
    12. Campbell J.F., Lewis E.E., Stock S.P., Nadler S., Kaya H.K. (2003): Evolution of host search strategies in entomopathogenic nematodes. Journal of Nematology, 35: 142-145. Go to PubMed...
    13. Cheng A.X., Xiang C.Y., Li J.X., Yang C.Q., Hu W.L., Wang L.J., Lou Y.G., Chen X.Y. (2007): The rice (E)-βcaryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry, 68: 1632-1641. Go to original source... Go to PubMed...
    14. Crespo E., Hordijk C.A., de Graff R.M., Samudrala D., Cristescu S.M., Harren F.J.M., van Dam N.M., (2012): On-line detection of root-induced volatiles in Brassica nigra plants infested with Delia radicum L. root fly larvae. Phytochemistry, 84: 68-77. Go to original source... Go to PubMed...
    15. Crocoll C., Asbach J., Novak J., Gershenzon J., Degenhardt J. (2010): Terpene synthases of oregano (Origanum vulgare L.) and their roles in the pathway and regulation of terpene biosynthesis. Plant Molecular Biology, 73: 587-603. Go to original source... Go to PubMed...
    16. Cruz-Martínez H., Ruiz-Vega J., Matadamas-Ortíz P.T., Cortés-Martínez C.I., Rosas-Diaz, J. (2017): Formulation of entomopathogenic nematodes for crop pest control - a review. Plant Protection Science, 53: 15-24. Go to original source...
    17. Degenhardt J. (2009): Indirect defense responses to herbivory in grasses. Plant Physiology, 149: 96-102. Go to original source... Go to PubMed...
    18. Degenhardt J., Gershenzon J., Baldwin I.T., Kessler A. (2003): Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Current Opinion in Biotechnology, 14: 169-176. Go to original source... Go to PubMed...
    19. De Nardo E.A.B., Grewal P.S. (2003): Compatibility of Steinernema feltiae (Nematoda: Steinernematidae) with pesticides and plant growth regulators used in glasshouse plant production. Biocontrol Science & Technology, 13: 441-448. Go to original source...
    20. Dicke M. (1999): Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomologia Experimentalis et Applicate, 91: 131-142. Go to original source...
    21. Dudareva N., Negre F., Nagegowda D.A., Orlova I. (2006): Plant volatiles: Recent advances and future perspectievs. Critical Reviews in Plant Sciences, 25: 417-440. Go to original source...
    22. Ehlers R.U. (1998): Entomopathogenic nematodes - save biocontrol agents for sustainable systems. Phytoprotection, 79: 94-102. Go to original source...
    23. Ehlers R.U. (2001): Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56: 523-633. Go to original source... Go to PubMed...
    24. Flores H.E., Vivanco J.M., Loyola-Vargas V.M. (1999): 'Radicle' biochemistry: The biology of root-specific metabolism. Trends in Plant Science, 4: 220-226. Go to original source... Go to PubMed...
    25. Fontana A., Held M., Fantaye C.A., Turlings T.C.J., Degenhardt J., Gershenzon J. (2011): Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). Journal of Chemical Ecology, 37: 582-591. Go to original source... Go to PubMed...
    26. Gaugler R., Campbell J.F. (1991): Selection for enhanced host-finding of scarab larvae (Coleoptera, Scarabaeidae) in an entomopathogenic nematode. Environmental Entomology, 20: 700-706. Go to original source...
    27. Gaugler R., Bednarek A., Campbell J.F. (1992): Ultraviolet inactivation of heterorhabditids and steinernematids. Journal of Invertebrate Pathology, 59: 155-160. Go to original source...
    28. Gaugler R., Campbell J.F., McGuire T.R. (1989): Selection for host-finding in Steinernema feltiae. Journal of Invertebrate Pathology, 54: 363-372. https://doi.org/10.17221/24/2019-PPS Go to original source...
    29. Georgis R., Koppenhöfer A.M., Lacey L.A., Bélair G., Duncan L.W., Grewal P.S., Samish M., Tan L., Torr P., van Tol R.W.H.M. (2006): Successes and failures in the use of parasitic nematodes for pest control. Biological Control, 38: 103-123. Go to original source...
    30. Glaser R.W., Farrell C.C. (1935): Field experiments with the Japanese beetle and its nematode parasite. Journal of New York Entomological Society, 43: 345-371.
    31. Glazer I., Klein M., Navon A., Nakache Y. (1992): Comparison of efficacy of entomopathogenic nematodes combined with antidesiccants applied by canopy sprays against three cotton pests (Lepidoptera: Noctuidae). Journal of Economic Entomology, 85: 1636-1641. Go to original source...
    32. Gosset V., Harmel N., Göbel C., Francis F., Haubruge E., Wathelet J.P., du Jardin P., Feussner I., Fauconnier M.L. (2009): Attacks by piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. Journal of Experimental Botany, 60: 1231-1240. Go to original source... Go to PubMed...
    33. Gouinguene S., Degen T., Turlings T.J.C. (2001): Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology, 11: 9-16. Go to original source...
    34. Grewal P.S., Gaugler R., Lewis E.E. (1993): Host recognition behaviour by entomopathogenic nematodes during contact within insect gut contents. Journal of Parasitology, 79: 495-503. Go to original source...
    35. Grewal P.S., Selvan S., Gaugler R. (1994): Thermal adaptation of entomopathogenic nematodes: niche breadth for infection, establishment, and reproduction. Journal of Thermal Biology, 19: 245-253. Go to original source...
    36. Griffin C.T., Downes M.J. (1994): Selection of Heterorhabditis sp. for improved infectivity at low temperatures. In: Burnell A.M., Ehlers R.U., Masson J.P. (eds): Genetics of Entomopathogenic Nematode-bacterium Complexes. Luxembourg, Office for Official Publications of the European Communities: 120-128.
    37. Hallem E.A., Dillman A.R., Hong A.V., Zhang Y.J., Yano J.M., DeMarco S.F., Sternberg P.W. (2011): A sensory code for host seeking in parasitic nematodes. Current Biology, 21: 377-383. Go to original source... Go to PubMed...
    38. Harvey J.A., Sano T., Tanaka T. (2010): Differential host growth regulation by the solitary endoparasitoid Meteorus pulchiornis in two hosts of greatly differing mass. Journal of Insect Physiology, 56: 1178-1183. Go to original source... Go to PubMed...
    39. Hassanali A., Herren H., Khan Z.R., Pickett J.A., Woodcock C.M. (2008): Integrated pest management: The push-pull approach for controlling insect pest and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philosophical Transactions of the Royal Society, 363: 611-621. Go to original source... Go to PubMed...
    40. Hazir S., Kaya H.K., Stock S.P., Keskin N. (2004): Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turkish Journal of Biology, 27: 181-202.
    41. Head J., Lawrence A.J., Walters K.F.A. (2004): Efficacy of the entomopathogenic nematode, Steinernema feltiae, against Bemisia tabaci in relation to plant species. Journal of Applied Entomology, 128: 543-547. Go to original source...
    42. Head J., Walters K.F.A., Langton S. (2000): The compatibility of the entomopathogenic nematode, Steinernema feltiae, and chemical insecticides for the control of the South American leafminer, Liriomyza huidobrensis. Biocontrol, 45: 345-353. Go to original source...
    43. Heil M. (2008): "Indirect defence via tritrophic interactions". New Phytologist, 178: 41-61. Go to original source... Go to PubMed...
    44. Hiltpold I., Turlings T.C.J. (2008): Belowground chemical signaling in maize: When simplicity rhymes with efficiency. Journal of Chemical Ecology, 34: 628-635. Go to original source... Go to PubMed...
    45. Hiltpold I., Erb M., Robert C.A.M., Turlings T.C.J. (2011): Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell and Environment, 34: 1267-1275. Go to original source... Go to PubMed...
    46. Hiltpold I., Toepfer S., Kuhlmann U., Turlings T.C.J. (2010c): How maize root volatiles influence the efficacy of entomopathogenic nematodes against the western corn rootworm? Chemoecology, 20: 155-162. Go to original source...
    47. Hiltpold I., Baroni M., Toepfer S., Kuhlmann U., Turlings T.C.J. (2010a): Selection of entomopathogenic nematodes for enhanced responsiveness to a volatile root signal helps to control a major root pest. Journal of Experimental Biology, 213: 2417-2423. Go to original source... Go to PubMed...
    48. Hiltpold I., Baroni M., Toepfer S., Kuhlmann U., Turlings T.C.J. (2010b): Selective breeding of entomopathogenic nematodes for enhanced attraction to a root signal did not reduce their establishment or persistence after field release. Plant Signalling and Behaviour, 5: 1450-1452. Go to original source... Go to PubMed...
    49. Hiltpold I., Bernklau E., Bjostad L.B., Alvarez N., MillerStruttmann N.E., Lundgren J.G., Hibbard B.E. (2013): Nature, evolution and characterisation of rhizospheric chemical exudates affecting root herbivores. In: Johnson S.N., Hiltpold I., Turlings T. (eds): Behaviour and Physiology of Root Herbivores. New York, Academic Press: 97-157. Go to original source...
    50. Ishibashi N., Choi D.R. (1991): Biological control of soil pests by mixed application of entomopathogenic and fungivorous nematodes. Journal of Nematology, 23: 175-181. Go to PubMed...
    51. Jagodiè A., Ipavec N., Trdan S., Laznik ®. (2017): Attraction behaviours: are synthetic volatiles, typically emitted by insect-damaged Brassica nigra roots, navigation signals for entomopathogenic nematodes (Steinernema and Heterorhabditis)? BioControl, 62: 515-524. Go to original source...
    52. Kaplan I. (2012): Attracting carnivorous arthropods with plant volatiles: The future of biocontrol or playing with fire? Biological Control, 60: 77-89. Go to original source...
    53. Kappers I.F., Ahroni A., van Herpen T.W., Luckerhoff L.L., Dicke M., Bouwmeester H.J. (2005): Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science, 309: 2070-2072. Go to original source... Go to PubMed...
    54. Kessler A., Baldwin I.T. (2002): Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology, 53: 299-328. Go to original source... Go to PubMed...
    55. Khan Z.R., Ampong-Nyarko K., Chiliswa P., Hassanali A., Kimani S., Lwande W., Overholt W.A., Pickett J.A., Smart L.E., Wadhams L.J. (1997): Intercropping increases parasitism of pests. Nature, 388: 631-632. Go to original source...
    56. Köllner T.G., Held M., Lenk C., Hiltpold I., Turlings T.J.C., Gershenzon J., Degenhardt J. (2008): A maize (E)-βcaryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell, 20: 482-494. Go to original source... Go to PubMed...
    57. Koppenhöfer A.M., Cowles R.S., Cowles E.A., Fuzy E.M., Baumgartner L. (2002): Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biological Control, 24: 90-97. Go to original source...
    58. Krishnayya P.V., Grewal P.S. (2002): Effect of neem and selected fungicides on viability and virulence of the entomopathogenic nematode Steinernema feltiae. Biocontrol Science and Technology, 12: 259-266. Go to original source...
    59. Laznik ®., Trdan S. (2011): Entomopathogenic nematodes (Nematoda: Rhabditida) in Slovenia: From tabula rasa to implementation into crop production systems. In: Perveen F.K. (ed.): Insecticides - Pest Engineering. Rijeka, InTechOpen: 627-656. Go to original source...
    60. Laznik ®., Trdan S. (2013): An investigation on the chemotactic responses of different entomopathogenic nematode strains to mechanically damaged root volatile compounds. Experimental Parasitology, 134: 349-355. Go to original source... Go to PubMed...
    61. Laznik ®., Trdan S. (2014): The influence of insecticides on the viability of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) under laboratory conditions. Pest Management Science, 70: 784-789. Go to original source... Go to PubMed...
    62. Laznik ®., Trdan S. (2016a): Attraction behaviors of entomopatogenic nematodes (Steinernematidae and Heterorhabditidae) to synthetic volatiles emitted by insect damaged carrot roots. Journal of Pest Science, 4: 977-984. Go to original source...
    63. Laznik ®., Trdan S. (2016b): Attraction behaviours of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) to synthetic volatiles emitted by insect damaged potato tubers. Journal of Chemical Ecology, 42: 314-322. Go to original source... Go to PubMed...
    64. Laznik ®., Trdan S. (2018): Are synthetic volatiles, typically emitted by insect-damaged peach cultivars, navigation signals for two-spotted lady beetle (Adalia bipunctata L.) and green lacewing (Chrysoperla carnea [Stephens]) larvae? Journal of Plant Diseases and Protection, 125: 529-538. Go to original source...
    65. Laznik ®., Ko¹ir I.J., Rozman L., Kaè M., Trdan S. (2011): Preliminary results of variability in mechanical-induced volatile root-emissions of different maize cultivars. Maydica, 56: 343-350.
    66. Laznik ®., Tóth T., Lakatos T., Vidrih M., Trdan S. (2010): Control of the Colorado potato beetle (Leptinotarsa decemlineata [Say]) on potato under field conditions: A comparison of the efficacy of foliar application of two strains of Steinernema feltiae (Filipjev) and spraying with thiametoxam. Journal of Plant Diseases and Protection, 117: 129-135. Go to original source...
    67. Lello E.R., Patel M.N., Mathews G.A., Wright D.J. (1996): Application technology for entomopathogenic nematodes against foliar pests. Crop Protection, 15: 567-574. Go to original source...
    68. Lewis E.E. (2002): Behavioural ecology. In: Gaugler R. (ed.): Entomopathogenic Nematology. Wallingford, CABI Publishing: 205-223. Go to original source...
    69. Loughrin J., Manukian A., Heath R., Tumlinson J. (1995): Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. Journal of Chemical Ecology, 21: 1217-1227. Go to original source... Go to PubMed...
    70. Majiæ I., Sarajliæ A., Lakatos T., Tóth T., Raspudiæ E., Pu¹kadija Z., Kani¾ai ©ariæ G., Laznik ®. (2019): Virulence of new strain of Heterorhabditis bacteriophora from Croatia against Lasioptera rubi. Plant Protection Science, 55: 134-141. Go to original source...
    71. Maron J.L., Kauffman M.J. (2006): Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology, 87: 113-124. Go to original source... Go to PubMed...
    72. O'Halloran D.M., Burnell A.M. (2003): An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora. Parasitology, 127: 375-385. Go to original source... Go to PubMed...
    73. Pickett J.A., Bruce T.J.A., Chamberlain K., Hassanali A., Khan Z.R., Matthes M.C., Napier J.A., Smart L.E., Wadhams L.J., Woodcock C.M. (2006): Plant volatiles yielding new ways to exploit plant defence. In: Dicke M., Takken W. (eds): Chemical Ecology: From Gene to Ecosystem. Dordrecht, Springer: 161-173. Go to original source...
    74. Poinar G.O., Grewal P.S. (2012): History of entomopathogenic nematology. Journal of Nematology, 44: 153-161. Go to PubMed...
    75. Pù¾a V. (2015): Control of insect pests by entomopathogenic nematodes. In: Lugtenberg B. (ed.): Principles of Plant-microbe Interactions. Cham, Springer International Publishing: 175-183. Go to original source...
    76. Rasmann S., Turlings T.C.J. (2008): First insights into specificity of belowground tritrophic interactions. Oikos, 117: 362-369. https://doi.org/10.17221/24/2019-PPS Go to original source...
    77. Rasmann S., Hiltpold I., Ali J. (2012): The role of root-produced volatile secondary metabolites in mediating soil interactions. In: Montanaro G., Cichio B. (eds): Advances in Selected Plant Physiology Aspects. Rijeka, InTech: 269-290. Go to original source...
    78. Rasmann S., Erwin A.C., Halitschke R., Agrawal A.A. (2011): Direct and indirect root defences of milkweed (Asclepias syriaca): Trophic cascades, trade-offs and novel methods for studying subterranean herbivory. Journal of Ecology, 99: 16-25. Go to original source...
    79. Rasmann S., Köllner T.G., Degenhardt J., Hiltpold I., Toepfer S., Kuhlmann U., Gershenzon J., Turlings T.C.J. (2005): Recruitment of entomopathogenic nematodes by insectdamaged maize roots. Nature, 434: 732-737. Go to original source... Go to PubMed...
    80. Robert C.A.M., Zhang X., Machado R.A.R., Schirmer S., Lori M., Mateo P., Erb M., Gershenzon J. (2017): Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels. eLife, 6: e29307. doi: 10.7554/eLife.29307 Go to original source... Go to PubMed...
    81. Rovesti L., Deseö K.V. (1990): Compatibility of chemical pesticides with the entomopathogenic nematodes, Steinernema carpocapsae Weiser and S. feltiae Filipjev (Nematoda: Steinernematidae). Nematologica, 36: 237-245. Go to original source...
    82. Schnee C., Köllner T.G., Held M., Turlings T.J.C., Gershenzon J., Degenhardt J. (2006): The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proceedings of the National Academy of Sciences of the United States of America, 103: 1129-1134. Go to original source... Go to PubMed...
    83. Schroer S., Ziermann D., Ehlers R.U. (2005): Mode of action of a surfactant-polymer formulation to support performance of the entomopathogenic nematode Steinernema carpocapsae for control of diamondback moth larvae (Plutella xylostella). Biocontrol Science and Technology, 15: 601-613. Go to original source...
    84. Shapiro-Ilan D.I., Lewis E.E., Tedders W.L. (2003): Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. Journal of Invertebrate Pathology, 83: 270-272. Go to original source... Go to PubMed...
    85. Shapiro-Ilan D.I., Gouge D.H., Piggott S.J., Fife J.P. (2006): Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control, 38: 124-133. Go to original source...
    86. Shapiro-Ilan D., Lewis E.E., Campbell J.F., Kim-Shapiro D.B. (2012): Directional movement of entomopathogenic nematodes in response to electrical field: Effect of species, magnitude of voltage, and infective juvenile age. Journal of Invertebrate Pathology, 109: 34-40. Go to original source... Go to PubMed...
    87. Sher R.B., Parella M.P. (1999): Biological control of the leafminer, Liriomyza trifolii, in chrysanthemums: Implications for intraguild predation between Diglyphus begini and Steinernema carpocapsae. Bulletin of the International Organization for Biological and Integrated Control of Noxious Animals and Plants: Integrated Control in Glasshouses, 22: 221-224.
    88. Smits P.S. (1996): Post-application persistence of entomopathogenic nematodes. Biocontrol Science and Technology, 6: 379-387. Go to original source...
    89. Toepfer S., Haye T., Erlandson M., Goettel M., Lundgren J.G., Kleespies R.G., Weber D.C., Walsh G.C., Peters A., Ehlers R.U., Strasser H., Moore D., Keller S., Vidal S., Kuhlmann U. (2009): A review of the natural enemies of beetles in the subtribe Diabroticina (Coleoptera: Chrysomelidae): Implications for sustainable pest management. Biocontrol Science and Technology, 19: 1-65. Go to original source...
    90. Turlings T.C.J., Ton J. (2006): Exploiting scents of distress: The prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Current Opinion in Plant Biology, 9: 421-427. Go to original source... Go to PubMed...
    91. Turlings T.C.J., Hiltpold I., Rasmann S. (2012): The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil, 359: 51-60. Go to original source...
    92. Turlings T.C.J., Tumlinson J.H., Lewis W.J. (1990): Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250: 1251-1253. Go to original source... Go to PubMed...
    93. van Tol R.W.H.M., van der Sommen A.T.C., Boff M.I.C., van Bezooijen J., Sabelis M.W., Smits P.H. (2001): Plants protect their roots by alerting the enemies of grubs. Ecology Letters, 4: 292-294. Go to original source...
    94. Vieira C.R., Blassioli Moras M.C., Borges M., Sujii E.R., Laumann R.A. (2013): cis-Jasmone indirect action on egg parasitoids (Hymenoptera: Scelionidae) and its application in biological control of soybean stink bugs (Hemiptera: Pentatomidae). Biological Control, 64: 75-82. Go to original source...
    95. Voglar G.E., Mrak T., Kri¾man M., Jagodiè A., Trdan S., Laznik ®. (2019): Effect of contaminated soil on multitrophic interactions in a terrestrial system. Plant and Soil, 435: 337-351. Go to original source...
    96. von Mérey G., Veyrat N., Mahuku G., Valdez R.L., Turlings T.J.C., D'Alessandro M. (2011): Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpens by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry, 72: 1838-1847. Go to original source... Go to PubMed...
    97. von Mérey G., Veyrat N., Mahuku G., Valdez R.L., Turlings T.J.C., D'Alessandro M. (2012): Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodopetra frugiperda in Mexican maize fields. Biological Control, 60: 7-15. Go to original source...
    98. Wang Y., Gaugler R. (1998): Host and penetration site location by entomopathogenic nematodes against Japanese beetle larvae. Journal of Invertebrate Pathology, 72: 313-318. Go to original source... Go to PubMed...
    99. Wenke K., Kai M., Piechulla B. (2010): Belowground vola-tiles facilitate interactions between plant roots and soil organisms. Planta, 231: 499-506. Go to original source... Go to PubMed...
    100. Wilson M.J., Ehlers R.U., Glazer I. (2012): Entomopathogenic nematode foraging strategies - is Steinernema carpocapsaereally an ambush forager? Nematology, 14: 389-394. Go to original source...
    101. Wright D.J., Peters A., Schroer S., Fife J.P. (2005): Application technology. In: Grewal P.S., Ehlers R.U., Shapiro-Ilan D.I. (eds): Nematodes as Biocontrol Agents. Wallingford, CABI Publishing: 91-106. Go to original source...
    102. Xiao Y., Wang Q., Erb M., Turlings T.J.C., Ge L., Hu L., Li J., Han X., Zhang T., Lu J. (2012): Specific herbivore-induced volatiles defend plants and determine insect community composition on the field. Ecology Letters, 15: 1130-1139. Go to original source... Go to PubMed...

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