Biological alternatives to pesticides to control wireworms (Coleoptera: Elateridae)

[en] Most studies on plant-insect interactions focus on the aboveground parts of plants, but the knowledge regarding the belowground interactions is increasing. Soil pests are at least equally dangerous to plant health and elicit plant defense mechanisms as well. Wireworms (Coleoptera: Elateridae) are common polyphagous soil pests of various crops, including economically relevant crops such as maize and potatoes. Their management with pesticides is often not successful or sustainable, and more research on biological alternatives is required. We aim at providing an overview of biological control methods under development or commercially available. Little is known about the natural enemies of wireworms, and the available work is often limited to laboratory experiments. The interest for using using microorganisms as biocontrol agent is increasing, and entomopathogenic fungi, nematodes, and bacteria represent promising alternatives to pesticides. The review discusses the combination of attractive semiochemicals with biological agents to improve wireworm monitoring and control, as well as research advances on these fronts

Disciplines :

Entomology & pest control

Author, co-author :

La Forgia, Diana ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Verheggen, François ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Language :

English

Title :

Biological alternatives to pesticides to control wireworms (Coleoptera: Elateridae)

Publication date :

2019

Journal title :

Agri Gene

Volume :

Peer reviewed :

Peer reviewed

Available on ORBi :

since 31 January 2019

Statistics

Number of views

199 (13 by ULiège)

Number of downloads

6 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Adams, R.G., Murray, K.D., Los, L.M., Effectiveness and selectivity of sex pheromone lures and traps for monitoring fall armyworm (Lepidoptera: Noctuidae) adults in Connecticut sweet corn. J. Econ. Entomol. 82 (1989), 285–290.
J.G. Ali, H.T. Alborn, L.L. Stelinski, Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes, J. Chem. Ecol. 36 (142) 361–368.
Allen, D.C., Abrahamson, L.P., Eggen, D.A., Lanier, G.N., Swier, S.R., Kelley, R.S., Auger, M., Monitoring spruce budworm (Lepidoptera: Tortricidae) populations with pheromone-baited traps. Environ. Entomol. 15 (1986), 152–165.
Ansari, M.A., Evans, M., Butt, T.M., Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Prot. 28 (2009), 269–272.
Baker, T.C., Staten, R.T., Flint, H.M., Use of pink bollworm pheromone in the southwestern United States. Behavior-Modifying Chemicals for Insect Management: Applications of Pheromones and Other Attractants, 1990, 417–436.
Balkov, V.I., Attractant traps for control of wireworms. Zashchita Rastenii (Moskova). 5 (1991), 24–25.
Barsics, F., Latine, R., Gfeller, A., Laloux, M., Lognay, G., Wathelet, J.P., Haubruge, E., Verheggen, F.J., Do root-emitted volatile organic compounds attract wireworms. Commun. Agric. Appl. Biol. Sci. 77 (2012), 561–565.
Barsics, F., Delory, B.M., Delaplace, P., Francis, F., Fauconnier, M.L., Haubruge, E., Verheggen, F.J., Foraging wireworms are attracted to root-produced volatile aldehydes. J. Pest. Sci. 90 (2017), 1–8.
Bezemer, T.M., van Dam, N.M., Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol. 20 (2005), 617–624.
Bird, A.F., Bird, J., Observations on the use of insect parasitic nematodes as a means of biological control of root-knot nematodes. Int. J. Parasitol. 16 (1986), 511–516.
Bischoff, J.F., Rehner, S.A., Humber, R.A., A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101 (2009), 512–530.
Borg-Karlson, A.K., Ågren, L., Dobson, H., Bergström, G., Identification and electroantennographic activity of sex-specific geranyl esters in an abdominal gland of female Agriotes obscurus (L.) and A. lineatus (L.)(Coleoptera, Elateridae). Cell. Mol. Life Sci. 44 (1988), 531–534.
Brandl, M.A., Schumann, M., Przyklenk, M., Patel, A., Vidal, S., S, Wireworm damage reduction in potatoes with an attract-and-kill strategy using Metarhizium brunneum. J. Pest. Sci. 90 (2017), 1–15.
Braun, A.R., van der Fliert, E., Evaluation of the impact of sweetpotato weevil (Cylas formicarius) and of the effectiveness of Cylas sex pheromone traps at the farm level in Indonesia. Int. J. Pest Manage. 45 (1999), 101–110.
Bravo, A., Likitvivatanavong, S., Gill, S.S., Soberón, M., Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41 (2011), 423–431.
Brown, V.K., Gange, A.C., Insect herbivory insect below ground. Adv. Ecol. Res. 20 (1990), 1–58.
Bruck, D.J., Snelling, J.E., Dreves, A.J., Jaronski, S.T., Laboratory bioassays of entomopathogenic fungi for control of Delia radicum (L.) larvae. J. Invertebr. Pathol. 89 (2005), 179–183.
Burghause, F., Schmitt, M., Monitoring of the Click-beetle Genus Agriotes (Elateridae, Coleoptera) in Rhineland-Palatinate in the years 2008 to 2010. Gesunde Pflanzen 63 (2011), 27–32.
Butler, L.I., McDonough, L.M., Onsager, J.A., Landis, B.J., Sex Pheromones of the Pacific Coast Wireworm, Limonius canus. Environ. Entomol. 4 (1975), 229–230.
Campos-Herrera, R., Gutiérrez, C., Screening Spanish isolates of steinernematid nematodes for use as biological control agents through laboratory and greenhouse microcosm studies. J. Invertebr. Pathol. 100 (2009), 100–105.
Campos-Herrera, R., El-Borai, F.E., Duncan, L.W., Wide interguild relationships among entomopathogenic and free-living nematodes in soil as measured by real time qPCR. J. Invertebr. Pathol. 111 (2012), 126–135.
Campos-Herrera, R., Jaffuel, G., Chiriboga, X., Blanco-Pérez, R., Fesselet, M., Půža, V., Mascher, F., Turlings, T.C.J., Traditional and molecular detection methods reveal intense interguild competition and other multitrophic interactions associated with native entomopathogenic nematodes in Swiss tillage soils. Plant Soil 389 (2015), 237–255.
Carde, R.T., Minks, A.K., Control of moth pests by mating disruption: successes and constraints. Annu. Rev. Entomol. 40 (1995), 559–585.
Chaston, J.M., et al. The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes. PLoS One, 6, 2011, e27909.
Collinge, W.E., Observations of the life-history and habits of Thereva nobilitata Fabr. and other species. J. Econ. Biol. 4 (1909), 14–18.
Conradi, A.F., Eagerton, H.C., Corn and Cotton Wireworm: (Horistonotus uhlerii, Horn), South Carolina Agricultural Experiment Station. 1914, 180.
Danismazoglu, M., Demir, I., Sevim, A., Demirbag, Z., Nalcacioglu, R., An investigation on the bacterial flora of Agriotes lineatus (Coleoptera: Elateridae) and pathogenicity of the flora members. Crop Prot. 40 (2012), 1–7.
De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R., Berg, M.P., de Ruiter, P.C., Verhoef, H.A., Bezemer, T.M., van der Putten, W.H., W, H., Soil invertebrate fauna enhances grassland succession and diversity. Nature 422 (2003), 711–713.
Dicke, M., Baldwin, I.T., The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help. Trends Plant Sci. 15 (2010), 167–175.
Doane, J.F., Evaluation of a Larval Trap and Baits for monitoring the Seasonal activity of Wireworms 1 in Saskatchewan 2. Environ. Entomol. 10 (1981), 335–342.
Doane, J.F., Klingler, J., Location of CO2-receptive sensilla on larvae of the wireworms Agriotes lineatus-obscurus and Limonius californicus. Ann. Entomol. Soc. Am. 71 (1978), 357–363.
Doane, J.F., Lee, Y.W., Klingler, J., Westcott, N.D., The orientation response of Ctemcera destructor and other wireworms (Coleoptera: Elateridae) to germinating grain and to carbon dioxide. Can. Entomol. 107 (1975), 1233–1252.
Domínguez, F., Los gusanos de alambre, Elatéridos de interés Agrícola. Bol. Patol. Veg. Entomol. Agr. 16 (1948), 119–156.
Duncan, L., Graham, J., Zellers, J., Bright, D., Dunn, D.C., El-Borai, F.E., Porazinska, D.L., Food web responses to augmenting the entomopathogenic nematodes in bare and animal manure-mulched soil. J. Nematol., 39, 2007, 176.
Eidt, D.C., Thurston, G.S., Physical deterrents to infection by entomopathogenic nematodes in wireworms (Coleoptera: Elateridae) and other soil insects. Can. Entomol. 127 (1995), 423–429.
Engel, E.O., Cuthbertson, A., On the immature stages of Psilocephala africana Wied. (Therevidae), together with a description of a species of Microstylum Macq. (Asilidae) new to science. T. Rhodesia Sci. Assn. 35 (1938), 132–135.
English, K.M.I., Notes on the morphology and biology of Anabarrhynchus fasciatus Macq. And other Australian Therevidae (Diptera, Therevidae). Proc. Linn. SocN. S. W. 75 (1950), 345–349.
Erb, M., Flors, V., Karlen, D., De Lange, E., Planchamp, C., D'Alessandro, M., Turlings, T.C.J., Ton, J., Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J. 59 (2009), 292–302.
Ericsson, J.D., Kabaluk, J.T., Goettel, M.S., Myers, J.H., Spinosad interacts synergistically with the insect pathogen Metarhizium anisopliae against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera: Elateridae). J. Econ. Entomol. 100 (2007), 31–38.
Ester, A., Huiting, H., Controlling Wireworms (Agriotes Spp.) in a Potato Crop with Biological, IOBC/Wprs Bul. Vol. 30, 2007, 189.
Faria, M., Hajek, A.E., Wraight, S.P., Imbibitional damage in conidia of the entomopathogenic fungi Beauveria bassiana, Metarhizium acridum and Metarhizium anisopliae. Biol. Control. 51 (2009), 346–354.
Filipchuk, O.D., Yaroshenko, V.A., Ismailov, V.Y., Vyatkina, G.G., Effectiveness of Biological and Chemical Preparations against Tobacco Pests, Agrokhimiya (Russian Federation). 1995.
Fox, C.J.S., The incidence of green muscardine in the European wireworm, Agriotes obscurus (Linnaeus), Nova Scotia. J. Insect Pathol. 3 (1961), 94–95.
Fox, C.J.S., Jaques, R.P., Note on the green-muscardine fungus, Metarhizium anisopliae (Metch.) Sor., as a control for wireworms. Can. Entomol. 90 (1958), 314–315.
Fox, C.J.S., MacLellan, C.R., Some Carabidae and Staphylinidae shown to feed on a wireworm, Agriotes sputator (L.), by the precipitin test. Can. Entomol. 88 (1956), 228–231.
Frank, J.H., Carabidae (Coleoptera) as predators of the red-backed cutworm (Lepidoptera: Noctuidae) in Central Alberta. Can. Entomol. 103 (1971), 1039–1044.
Furlan, L., Analisi delle possibilità di riduzione dell'impiego di geodisinfestanti nella coltura del mais nel Veneto, L'Info. Agra. 17 (1989), 107–115.
Furlan, L., Tóth, M., Yatsynin, V.G., Ujvary, I., The project to implement IPM strategies against Agriotes species in Europe: what has been done and what is still to be done. Proceedings of XXI IWGO Conference, Legnaro, Italy, 27, 2001, 253–262.
Gepp, J., Klausnitzer, B., Therevidenlarven (Dipt., Therevidae) als Prädatoren des Ameisenlöwen Euroleon nostras (Neuroptera, Myrmeleontidae). Entomol. Nachr. Ber. 49 (2005), 25–27.
Gillespie, A.T., Claydon, N., The use of entomopathogenous fungi for pest control and the role of toxins in pathogenesis. Pestic. Sci. 27 (1989), 203–215.
Gillespie, J.P., Bailey, A.M., Cobb, B., Vilcinskas, A., Fungi as elicitors of insect immune responses. Arch. Insect Biochem. Physiol. 44 (2000), 49–68.
Gorham, R.P., Notes on Agriotes mancus SAY, at Dartmouth. P. Acad. Entomol. Soc. 9 (1923), 69–72.
Greathead, D.J., A review of the insect enemies of Acridoidea (Orthoptera). Trans. R. Entomol. Soc. Lond. 114 (1963), 437–516.
Habtegebreiel, B., Getu, E., Dawd, M., Seyoum, E., Atenafu, G., Welde-Hawariat, Y., Ekesi, E., Hilbur, Y., Larsson, M., Field Level Auto-inoculation of Sorghum chafer, Pachnoda interrupta (Olivier)(Coleoptera: Scarabaedae) with Metarhizium anisopliae based Microbial Bio-control Agents using locally Affordable Traps. J. Biol. Control. 30 (2016), 68–77.
Hajek, A.E., Delalibera, J.I., Fungal pathogens as classical biological control agents against arthropods. BioControl 55 (2010), 147–158.
Hall, D.G., Insects and mites associated with sugarcane in Florida. Flo. Entomol., 1988, 138–150.
Hartmann, T., Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta 219 (2004), 1–4.
Hazir, S., Kaya, H.K., Stock, S.P., Keskin, N., Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turk. J. Biol. 27 (2004), 181–202.
Hildebrand, C.W., Morphological and ecological observations on the larvae of Therevidae (Diptera). Wasmann J. Biol. 10 (1952), 355–357.
Howse, P.E., Knapp, J.J., Pheromones of Mediterranean fruit fly: Presumed mode of action and implications for improved trapping techniques. Fruit Fly Pests: A World Assessment of their Biology and Management, 1996, St. Lucie Press, Delray Beach, Florida, 91–99.
Hoyt, S.C., Westigard, P.H., Rice, R.E., Development of pheromone trapping techniques for male San Jose scale (Homoptera: Diaspididae). Environ. Entomol. 12 (1983), 371–375.
Huxham, I.M., Lackie, A.M., McCorkindale, N.J.M., Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae, on cellular immunity in insects. J. Insect Physiol. 35 (1989), 97–105.
Hyslop, J.A., Wireworms attacking cereal and forage crops. USDA Bul., 156, 1915, 34.
Hywel-Jones, N.L., Gillespie, A.T., Effect of temperature on spore germination in Metarhizium anisopliae and Beauveria bassiana. Mycol. Res. 94 (1990), 389–392.
Jansson, R.K., Seal, D.R., Biology and management of wireworms on potato. Adv. in potato pest biol. and manage., 1994, 31–53.
Jenkins, J.W., Doane, C.C., Schuster, D.J., McLughlin, J.R., Jiménez, M., Development and commercial application of sex pheromone for control of the tomato pinworm. Behavior-Modifying Chemicals for Pest Management: Applications of Pheromones and Other Attractants, 1990, Marcel Dekker, New York, 269–280.
Johnson, S.N., Gregory, P.J., Chemically-mediated host-plant location and selection by root-feeding insects. Physiol. Entomol. 31 (2006), 1–13.
Johnson, S.N., Nielsen, U.N., Foraging in the dark–chemically mediated host plant location by belowground insect herbivores. J. Chem. Ecol. 38 (2012), 604–614.
Kabaluk, J.T., Ericsson, J.D., Seed treatment increases yield of field corn when applied for wireworm control. Agron. J. 99 (2007), 1377–1381.
Kabaluk, J.T., Goettel, M., Erlandson, M., Ericsson, J., Duke, G., Vernon, R., Metarhizium anisopliae as a biological control for wireworms and a report of some other naturally-occurring parasites. IOBC/wprs Bull. 28 (2005), 109–115.
Kabaluk, J.T., Lafontaine, J.P., Borden, J.H., An attract and kill tactic for click beetles based on Metarhizium brunneum and a new formulation of sex pheromone. J. Pest. Sci. 88 (2015), 707–716.
Kamm, J.A., Davis, H.G., McDonough, L.M., Attractants for several genera and species of wireworms (Coleoptera: Elateridae). The Coleopt. Bull., 1983, 16–18.
Karban, R., Baldwin, I.T., Induced Responses to Herbivory. 1997, University of Chicago Press.
Kaya, H.K., Lacey, L.A., Introduction to microbial control. Field Manual of Techniques in Invertebrate Pathology, 2000, Springer, Nederland, 1–4.
Kessler, A., Baldwin, I.T., Defensive function of herbivore-induced plant volatile emissions in nature. Science 291 (2001), 2141–2144.
Kleespies, R.G., Ritter, C., Zimmermann, G., Burghause, F., Feiertag, S., Leclerque, A., A survey of microbial antagonists of Agriotes wireworms from Germany and Italy. J. Pest. Sci. 86 (2013), 99–106.
Klein, M.G., Lacey, L.A., An attractant trap for autodissemination of entomopathogenic fungi into populations of the Japanese beetle Popillia japonica (Coleoptera: Scarabaeidae). Biocontrol Sci. Techn. 9 (1999), 151–158.
Kloepper, J.W., Schroth, M.N., Miller, T.D., Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology 70 (1980), 1078–1082.
Knight, A.L., Hilton, R., Light, D.M., Monitoring codling moth (Lepidoptera: Tortricidae) in apple with blends of ethyl (E, Z)-2, 4-decadienoate and codlemone. Environ. Entomol. 34 (2005), 598–603.
Koelliker, U., Biasio, L., Jossi, W., Potential control of Swiss wireworms with entomopathogenic fungi. IOBC/wprs Bulletin. 66 (2011), 517–520.
Kostenko, O., Mulder, P.P., Bezemer, T.M., Effects of root herbivory on pyrrolizidine alkaloid content and aboveground plant-herbivore-parasitoid interactions in Jacobaea vulgaris. J. Chem. Ecol. 39 (2013), 109–119.
Kudryavtsev, I., Siirde, K., Lääts, K., Ismailov, V., Pristavko, V., Determination of distribution of harmful click beetle species (Coleoptera: Elateridae) by synthetic sex pheromones. J. Chem. Ecol. 9 (1993), 1607–1611.
Kuhar, T.P., Doughty, H., Evaluation of foliar insecticides for the control of Colorado potato beetle in potatoes in Virginia. Arth. Manag. Tests., 2008, 33.
Kupferschmied, P., Maurhofer, M., Keel, C., Promise for plant pest control: root-associated pseudomonads with insecticidal activities. Front. Plant Sci., 4, 2013, 287.
Kurir, A., Über die Antagonisten der Fichtengespinstblattwespe, Cephaleia abietis L. (Hym. Pamphiliidae), im Bodenquarterier mit besonderer Berücksichtigung der Virulenz pathogener Pilze. Z. Angew. Entomol. 84 (1977), 388–396.
Lacey, L.A., Georgis, R., Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. J. Nematol., 44, 2012, 218.
Lacey, L.A., Fruto, R., Kaya, H.K., Vail, P., Insect pathogens as biological control agents: do they have a future?. Biol. Control 21 (2001), 230–248.
Lacey, L.A., Unruh, T.R., Simkins, H., Thomsen-Archer, K., Gut bacteria associated with the Pacific Coast wireworm, Limonius canus, inferred from 16s rDNA sequences and their implications for control. Phytoparasitica 35 (2007), 479–489.
Ladurner, E., Benuzzi, M., Fiorentini, F., Franceschini, S., Beauveria bassiana strain ATCC 74040 (Naturalis®), a valuable tool for the control of the cherry fruit fly Rhagoletis cerasi. Ecofruit-13th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing: Proceedings to the Conference from 18thFebruary to 20th February 2008 at Weinsberg, Germany, 2008, 93–97.
G.A. Langenbruch, N. Lorenz, A ten-year study on the applicability of pheromone-baited traps for monitoring the European corn borer (Ostrinia nubilalis Hbn.) in the Federal Republic of Germany. Part 1. Distribution of pheromone strains and testing of different trap types, baits and trap sites, Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz (Deutschland, FR), 1992.
Law, J.H., Regnier, F.E., Pheromones Annu. Rev. Biochem. 40 (1971), 533–548.
A. Leclerque A, R.G. Kleespies, C. Ritter, C. Schuster, S. Feiertag, Genetic and Electron-Microscopic Characterization of 'Rickettsiella agriotidis', a new Rickettsiella Pathotype Associated with Wireworm, Agriotes sp. (Coleoptera: Elateridae), Curr. Microbiol. 63 (2011) 158–163.
Levine, E., Spencer, J.L., Isard, S.A., Onstad, D.W., Gray, M.E., Adaptation of the western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), to crop rotation: evolution of a new strain in response to a cultural management practice. Am. Entomol. 48 (2002), 94–107.
Li, D.P., Holdom, D.G., Effect of soil matric potential on sporulation and conidial survival of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). J. Invertebr. Pathol. 62 (1993), 273–277.
Li, D.P., Holdom, D.G., Effects of nutrients on colony formation, growth, and sporulation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). J. Invertebr. Pathol. 65 (1995), 253–260.
Lilly, C.E., McGinnis, A.J., Quantitative responses of males of Limonius californicus (Coleoptera: Elateridae) to female sex pheromone. Can. Entomol. 100 (1968), 1071–1078.
Lundgren, J.G., Nichols, S., Prischmann, D.A., Ellsbury, M.M., Seasonal and diel activity patterns of generalist predators associated with Diabrotica virgifera immatures (Coleoptera: Chrysomelidae). Biocontrol Sci. Techn. 19 (2009), 327–333.
Lyytikäinen-Saarenmaa, P., Varama, M., Anderbrant, O., Kukkola, M., Hedenström, E., Högberg, H.E., Predicting Pine Sawfly Population Densities and Subsequent Defoliation with Pheromone Traps, Integrated Management and Dynamics of Forest Defoliating Insects. 2001, 108–116.
Macauley, E.D.M., Etheridge, P., Garthwaite, D.G., Greenway, A.R., Wall, C., Goodchild, R.E., Prediction of optimum spraying dates against pea moth (Cydia nigricana) using pheromone traps and temperature measurements. Crop Prot. 4 (1985), 85–98.
Mason, P.G., Gillespie, D.R., Biological Control Programmes in Canada 2001–2012. 2013, CABI.
Mason, J.M., Wright, D.J., Potential for the Control of Plutella xylostella larvae with Entomopathogenic Nematodes. J. Invertebr. Pathol. 70 (1997), 234–242.
Morton, A., Garcia-Del-Pino, F., Laboratory and field evaluation of entomopathogenic nematodes for control of Agriotes obscurus (L.)(Coleoptera: Elateridae). J. Appl. Entomol. 141 (2016), 241–246.
Nicolas, G., Sillans, D., Immediate and latent effects of carbon dioxide on insects. Annu. Rev. Entomol. 34 (1989), 97–116.
Nordlund, D.A., Semiochemicals: Their Role in Pest Control. 1981, Wiley, New York.
Omkar, Eco Friendly Pest Management for Food Security. 2016, Academic Press, San Diego.
Ourry, M., Lebreton, L., Chaminade, V., Guillerm-Erckelboudt, A.Y., Hervé, M., Linglin, J., Marnet, N., Ourry, A., Paty, C., Poinsot, D., Cortesero, A.M., Influence of Belowground Herbivory on the Dynamics of root and Rhizosphere Microbial Communities. Front. Ecol. Evol., 6, 2018, 91.
Parker, W.E., Howard, J.J., The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agric. Forest. Entomol. 3 (2001), 85–98.
Perry, R.N., Moens, M., Starr, J.L., Root-knot nematodes. 2009, CABI.
Pigott, C.R., Ellar, D.J., Role of receptors in Bacillus thuringiensis crystal toxin activity, Microbiol. Mol. Biol. Rev. 71 (2007), 255–281.
Pons, X., Lumbierres, B., Lopez, C., Albajes, R., Abundance of non-target pests in transgenic Bt-maize: a farm scale study. European Journal of Entomology, 102(1), 2005, 73.
Prischmann-Voldseth, D.A., Dashiell, K.E., Effects of releasing a generalist predator (Acari: Gaeolaelaps aculeifer) on a subterranean insect herbivore (Coleoptera: Diabrotica virgifera virgifera). Biol. Control 65 (2013), 190–199.
Rabb, R.L., Biology of Conoderus vespertinus in the Piedmont section of North Carolina (Coleoptera: Elateridae). Ann. Entomol. Soc. Am. 56 (1963), 669–676.
Rasmann, S., Agrawal, A.A., In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol. 146 (2008), 875–880.
Rasmann, S., Turlings, T.C.J., First insights into specificity of belowground tritrophic interactions. Oikos 117 (2008), 362–369.
Rasmann, S., Köllner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., Turlings, T.C.J., Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434 (2005), 732–737.
Rasmann, S., Bauerle, T.L., Poveda, K., Vannette, R., Predicting root defence against herbivores during succession. Funct. Ecol. 25 (2011), 368–379.
Reinecke, A., Müller, F., Hilker, M., Attractiveness of CO2 released by root respiration fades on the background of root exudates. Basic Appl. Ecol. 9 (2008), 568–576.
Robert, C.A.M., Veyrat, N., Glauser, G., Marti, G., Doyen, G.R., Villard, N., Gaillard, M.D.P., Köllner, T.G., Giron, D., Body, M., Babst, B.A., Ferrieri, R.A., Turlings, T.C.J., A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol. Lett. 15 (2012), 55–64.
L.P. Rockwood, Entomogenous fungi of the Genus Metahizium on wireworms in the Pacific Northwest, Annu. Entomol. Soc. Am. 43 (1) 495–498.
Rodriguez-Saona, C., Blaauw, B.R., Isaacs, R., Manipulation of Natural Enemies in Agroecosystems: Habitat and Semiochemicals for Sustainable Insect Pest Control, in: Integrated Pest Management and Pest Control-Current and Future Tactics. 2012, InTech, 89–126.
Ruiu, L., Satta, A., Floris, I., Emerging entomopathogenic bacteria for insect pest management. Bull. Insectol. 66 (2013), 181–186.
Sabels, M.W., Dicker, M., Long-Range Dispersal and Searching Behavior, in: Spider Mites, their Biology Natural Enemies and Control. 1985, Elsevier, Amsterdam, 141–160.
G. Sanahuja, R. Banakar, R.M. Twyman, T. Capell, P. Christou, Bacillus thuringiensis: a century of research, development and commercial applications, Plant Biotechnol. J. 9 (71) 283–300.
Schalk, J.M., Bohac, J.R., Dukes, P.D., Martin, W.R., Potential of non-chemical control strategies for reduction of soil insect damage in sweetpotato. J. Am. Soc. Hortic. Sci. 118 (1993), 605–608.
Schmidt, J., All, J.N., Chemical attraction of Neoaplectana carpocapsae (Nematoda: Steinernematidae) to insect larvae. Environ. Entomol. 7 (1978), 605–607.
Schumann, M., Ladin, Z.S., Beatens, J.M., Hiltpold, I., Navigating on a chemical radar: Usage of root exudates by foraging Diabrotica virgifera virgifera larvae. J. Appl. Entomol. 142:10 (2018), 911–920.
Shapiro-Ilan, D.I., Han, R., Dolinksi, C., Entomopathogenic nematode production and application technology. J. Nematol. 44 (2012), 206–217.
Stubbs, A.E., Drake, M., British Soldierflies and their allies an illustrated guide to their identification and ecology. 2001, Brit. Entomo. and Nat. Hist. Society, Reading, UK.
Sufyan, M., Neuhoff, D., Furlan, L., Assessment of the range of attraction of pheromone traps to Agriotes lineatus and Agriotes obscurus. Agricul. Forest. Entomol. 13 (2011), 313–319.
Tanada, Y., Kaya, H.K., Insect Pathology. 1993, Academic Press, San Diego.
Tapia, T., Peric, F., Pardo, F., Palma, G., Quiroz, A., Identification of volatiles from differently aged red clover (Trifolium pratense) root extracts and behavioural responses of clover root borer (Hylastinus obscurus)(Marsham)(Coleoptera: Scolytidae) to them. Biochem. Syst. Ecol. 35 (2007), 61–67.
Tharp, C.I., Blodgett, S.L., Jaronski, S., Control of wireworms (Elateridae) in potatoes with microbial Metarhizium. Arth. Manag. Tests., 32, 2007.
Tinline, R.D., Zacharuk, R.Y., Pathogenicity of Metarrhizium anisopliae (Metch.) Sor. And Beauveria bassiana (Bals.) Vuill. to two species of Elateridae. Nature 187 (1960), 794–795.
Toba, H.H., Lindegren, J.E., Turner, J.E., Vail, P.V., Susceptibility of the Colorado potato beetle and the sugarbeet wireworm to Steinernema feltiae and S. glaseri. J. Nematol., 15(4), 1983, 597.
Tóth, M., Pheromones and attractants of click beetles: an overview. J. Pest. Sci. 86 (2013), 3–17.
Toth, M., Furlan, L., Yatsynin, V.G., Ujvary, I., Szarukan, I., Imrei, Z., Tolasch, T., Francke, W., Jossi, W., Identification of pheromones and optimization of bait composition for click beetle pests (Coleoptera: Elateridae) in Central and Western Europe. Pest Manag. Sci. 59 (2003), 417–425.
Traugott, M., Benefer, C.M., Blackshaw, R.P., van Herk, W.G., Vernon, R.S., Biology, ecology, and control of elaterid beetles in agricultural land. Annu. Rev. Entomol. 60 (2015), 313–334.
Turlings, T.C.J., Benrey, B., Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5 (1998), 321–333.
van Dam, N.M., Belowground herbivory and plant defenses. Annu. Rev. Ecol. Evol. Syst. 40 (2009), 373–391.
van Dam, N.M., Bouwmeester, H.J., Metabolomics in the rhizosphere: Tapping into belowground chemical communication. Trends Plant Sci. 21 (2016), 256–265.
van Herk, W.G., Vernon, R.S., Cronin, E.M.L., Gaimari, S.D., Predation of Thereva nobilitata (Fabricius)(Diptera: Therevidae) on Agriotes obscurus L. (Coleoptera: Elateridae). J. Appl. Entomol. 139 (2015), 154–157.
Vänninen, I., Hokkanen, H., Tyni-Juslin, J., Screening of field performance of entomopathogenic fungi and nematodes against cabbage root flies (Delia radicum L. and D. floralis (fall.); Diptera, Anthomyiidae). Acta Agriculturae Scandinavica B 49 (1999), 167–183 Plant Soil Sci.
Vernon, R.S., van Herk, W.G., Wireworms as pests of potato. Insect Pests of Potato: Global Perspec, Tives on Biology and Management, 2013, Elsevier, Amsterdam, 103–164.
Wardle, D.A., D, A., The influence of biotic interactions on soil biodiversity. Ecol. Lett. 9 (2006), 870–886.
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., Van Der Putten, W.H., Wall, D.H., Ecological linkages between aboveground and belowground biota. Science 304 (2004), 1629–1633.
Witzgall, P., Kirsch, P., Cork, A., Sex pheromones and their impact on pest management. J. Chem. Ecol. 36 (2010), 80–100.
Wraight, S.P., Lacey, L.A., Kabaluk, J.T., Goettel, M.S., Potential for microbial biological control of Coleopteran and Hemipteran pests of potato. Fruit Veg. Cereal Sci. Biotech. 3 (2009), 25–38.
R.D. Yanai, D.M. Eissenstat, Coping with herbivores and pathogens: a model of optimal root turnover, Funct. Ecol. 16 (202) 865–869.
Yatsynin, V.G., Rubanova, E.V., Okhrimenko, N.V., Identification of female-produced sex pheromones and their geographical differences in pheromone gland extract composition from click beetles (Coleoptera: Elateridae). J. Appl. Entomol. 120 (1996), 463–466.
Zacharuk, R.Y., Penetration of the cuticular layers of elaterid larvae (Coleoptera) by the fungus Metarrhizium anisopliae, and notes on a bacterial invasion. J. Invertebr. Pathol. 21 (1973), 101–106.
Zacharuk, R.Y., Tinline, R.D., Pathogenicity of Metarhizium anisopliae, and other fungi, for five elaterids (Coleoptera) in Saskatchewan. J. Invertebr. Pathol. 12 (1968), 294–309.
Zhang, F., Toepfer, S., Riley, K., Kuhlmann, U., Reproductive biology of Celatoria compressa (Diptera: Tachinidae), a parasitoid of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Biocontrol Sci. Techn. 14 (2004), 5–16.
Zhao, K.J., Zhang, L.K., Song, J., Zhang, L.H., Li, G.X., Wang, X.Y., Wang, Y., On the application of steinernematid nematodes against eight lepidopterous and coleopterous insect pests. Acta Phytophyl. Sin. 23 (1996), 20–22.