Alternative Strategies for Controlling Wireworms in Field Crops: A Review
Abstract
:1. Introduction
2. Risk Assessment
2.1. Evaluation of Risk Factors
2.1.1. Risk Factors
Risk Factor | Potential for Increasing Damage Risk | Factor Effect | Reference |
---|---|---|---|
Climate | |||
Soil temperature | Medium–High | ↑ T °C before seeding ⇒ ↓ damage risk and ~12 °C threshold (Agriotes spp. in maize) ↑ T °C ⇒ ↑ total abundance of wireworm community in cereals, Northern USA ↑ T °C ⇒ ↓ abundance of S. pruininus in cereals | [21,22,24,25,53] |
Rainfall | Medium | Depends on the species and the period under consideration | [22,23,24,25] |
Soil properties | |||
Organic matter content | Medium–High | ↑ OM ⇒ ↑ risk High risk when OM>5% (Agriotes spp.) | [23,24,25,52] |
Soil moisture | Medium–High | ↑mean frequency of days above a moisture threshold ⇒ ↓ wireworm occurrence (IA, USA) Soil-dependent | [21,22] |
pH | Medium | Low pH ⇒ ↑ damage risk in maize (Agriotes spp.) Increased abundance in L. californicus with higher soil pH | [24,25,53] |
Texture | Low | Loam soil ⇒ ↓ damage risk | [22,23,24,25,52,53] |
Drainage | Medium | Bad drainage ⇒ ↓ damage risk | [23,25] |
Current agricultural practices | |||
Sowing date | Medium | Late sowing (maize) ⇒ ↑ risk | [23,25,52] |
Tillage | Medium–High | Ploughing during summer ⇒ ↓ damage risk in sweet potato | [54] |
Fertilizer application | Low | Slight decrease in damage caused by Agriotes spp. in maize if fertilization compared to none | [25] |
Past agricultural practices | |||
Tillage | Medium–High | Intense tillage decreases damage risk compared to reduced tillage | [55] |
Field configuration | |||
Topography | Low | No significant effect | [25,32] |
Exposition | Low | Very weak difference in damage caused by Agriotes spp. in maize | [25,32] |
Field history | |||
Historic of meadows | High | Long-lasting meadow favorable to wireworm damage in maize (community of Agriotes species) | [23,25,52] |
Crop rotation type | High | Rotation including meadows and second crops ⇒ ↑damage risk in maize (Agriotes spp.) | [23,25,52] |
Landscape context | |||
Meadow (or grassy field margins) adjacency | Medium | Presence of adjacent meadow ⇒ ↑ risk | [23,25,52,56] |
Species occurrence | |||
Species identity | High | Level of damage in maize fields in Italy: A.brevis most harmful, then A. sordidus and A. ustulatus Different best predictors in Agriotes wireworm abundance in Croatia. E.g.: A. brevis→previous crop grown; A. sputator→rainfall; A. ustulatus→soil pH and humus Different predictors of wireworm abundance in northern US cereal fields. E.g.: L. infuscatus→crop type and soil texture; L. californicus → crop type, soil moisture, and soil pH | [24,35,53] |
2.1.2. Decision-Support Systems
2.2. Monitoring and Thresholds
2.2.1. Adult Monitoring
2.2.2. Larval Monitoring
2.2.3. IPM Thresholds
3. Pest Population Management
3.1. Cultural or Mechanical Control
3.1.1. Effect of Rotation
3.1.2. Effect of Tilling
3.1.3. Effect of Water Management
3.2. Semiochemical Control
3.3. Biological Control of Wireworms
3.3.1. Wireworm Predators
3.3.2. Wireworm Parasitoids and Parasites
3.3.3. Hymenoptera
3.3.4. Nematodes
3.3.5. Fungi
3.3.6. EPN and EPF Use Generally
3.3.7. Attract and Kill—A Possible Solution?
3.3.8. Problem: Different Species of Wireworms
3.4. Naturally Derived Insecticides
3.5. Habitat Manipulation
4. Crop Damage Management
4.1. Cultural Control
4.1.1. Optimal Sowing and Harvest Timing
4.1.2. Resistant Varieties
4.2. Pest Behavior Manipulation: Feeding Pest as an IPM Strategy
4.2.1. Trap Crops
4.2.2. Companion Plants: Feeding Pests as an IPM Strategy
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Hallmann, C.A.; Sorg, M.; Jongejans, E.; Siepel, H.; Hofland, N.; Schwan, H.; Stenmans, W.; Müller, A.; Sumser, H.; Hörren, T.; et al. More than 75 Percent Decline over 27 Years in Total Flying Insect Biomass in Protected Areas. PLoS ONE 2017, 12, e0185809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seibold, S.; Gossner, M.M.; Simons, N.K.; Blüthgen, N.; Müller, J.; Ambarlı, D.; Ammer, C.; Bauhus, J.; Fischer, M.; Habel, J.C.; et al. Arthropod Decline in Grasslands and Forests Is Associated with Landscape-Level Drivers. Nature 2019, 574, 671–674. [Google Scholar] [CrossRef] [PubMed]
- Vogel, G. Where Have All the Insects Gone? Science 2017, 356, 576–579. [Google Scholar] [CrossRef] [PubMed]
- Pisa, L.; Goulson, D.; Yang, E.-C.; Gibbons, D.; Sánchez-Bayo, F.; Mitchell, E.; Aebi, A.; van der Sluijs, J.; MacQuarrie, C.J.K.; Giorio, C.; et al. An Update of the Worldwide Integrated Assessment (WIA) on Systemic Insecticides. Part 2: Impacts on Organisms and Ecosystems. Environ. Sci. Pollut. Res. 2017. [Google Scholar] [CrossRef] [Green Version]
- Labrie, G.; Gagnon, A.-È.; Vanasse, A.; Latraverse, A.; Tremblay, G. Impacts of Neonicotinoid Seed Treatments on Soil-Dwelling Pest Populations and Agronomic Parameters in Corn and Soybean in Quebec (Canada). PLoS ONE 2020, 15, e0229136. [Google Scholar] [CrossRef]
- Balachowsky, A.; Mesnil, L. Les taupins. In Les Insectes Nuisibles aux Plantes Cultivées; Balachowsky, A., Ed.; Presses éts Busson: Paris, France, 1935; pp. 754–787. [Google Scholar]
- Veres, A.; Wyckhuys, K.A.G.; Kiss, J.; Tóth, F.; Burgio, G.; Pons, X.; Avilla, C.; Vidal, S.; Razinger, J.; Bazok, R.; et al. An Update of the Worldwide Integrated Assessment (WIA) on Systemic Pesticides. Part 4: Alternatives in Major Cropping Systems. Environ. Sci. Pollut. Res. 2020. [Google Scholar] [CrossRef]
- Furlan, L. An IPM Approach Targeted against Wireworms: What Has Been Done and What Has to Be Done. IOBC/WPRS Bull. 2005, 28, 91–100. [Google Scholar]
- Furlan, L. The Biology of Agriotes Ustulatus Schaller (Col., Elateridae). II. Larval Development, Pupation, Whole Cycle Description and Practical Implications. J. Appl. Entomol. 1998, 122, 71–78. [Google Scholar] [CrossRef]
- Furlan, L. The Biology of Agriotes Sordidus Illiger (Col., Elateridae). J. Appl. Entomol. 2004, 128, 696–706. [Google Scholar] [CrossRef]
- Miles, H.W. Wireworms and Agriculture, with Special Reference to Agriotes Obscurus L. Ann. Appl. Biol. 1942, 29, 176–180. [Google Scholar] [CrossRef]
- Sufyan, M.; Neuhoff, D.; Furlan, L. Larval Development of Agriotes Obscurus under Laboratory and Semi-Natural Conditions. Bull. Insectol. 2014, 67, 227–235. [Google Scholar]
- Lehmhus, J.; Niepold, F. Identification of Agriotes Wireworms—Are They Always What They Appear to Be? J. Cultiv. Plants 2015, 67, 129–138. [Google Scholar]
- Zacharuk, R.Y. Seasonal Behavior of Larvae of Ctenicera Spp. and Other Wireworms (Coleoptera:Elateridae), in Relation to Temperature, Moisture, Food, and Gravity. Can. J. Zool. 1962, 40, 697–718. [Google Scholar] [CrossRef]
- Barzman, M.; Bàrberi, P.; Birch, A.N.E.; Boonekamp, P.; Dachbrodt-Saaydeh, S.; Graf, B.; Hommel, B.; Jensen, J.E.; Kiss, J.; Kudsk, P.; et al. Eight Principles of Integrated Pest Management. Agron. Sustain. Dev. 2015, 35, 1199–1215. [Google Scholar] [CrossRef]
- Campbell, R.E. Temperature and Moisture Preferences of Wireworms. Ecology 1937, 18, 479–489. [Google Scholar] [CrossRef]
- Lafrance, J. The Seasonal Movements of Wireworms (Coleoptera: Elateridae) in Relation to Soil Moisture and Temperature in the Organic Soils of Southwestern Quebec. Can. Entomol. 1968, 100, 801–807. [Google Scholar] [CrossRef]
- Kovacs, T.; Kuroli, G.; Pomsar, P.; Német, L.; Pali, O.; Kuroli, M. Localisation and Seasonal Positions of Wireworms in Soils. Commun. Agric. Appl. Biol. Sci. 2006, 71, 357–367. [Google Scholar]
- Evans, A.C.; Gough, H.C. Observations on Some Factors Influencing Growth in Wireworms of the Genus Agriotes Esch. Ann. Appl. Biol. 1942, 29, 168–175. [Google Scholar] [CrossRef]
- Furlan, L. The Biology of Agriotes Ustulatus Schäller (Col., Elateridae). I. Adults and Oviposition. J. Appl. Entomol. 1996, 120, 269–274. [Google Scholar] [CrossRef]
- Jung, J.; Racca, P.; Schmitt, J.; Kleinhenz, B. SIMAGRIO-W: Development of a Prediction Model for Wireworms in Relation to Soil Moisture, Temperature and Type. J. Appl. Entomol. 2014, 138, 183–194. [Google Scholar] [CrossRef]
- Lefko, S.A.; Pedigo, L.P.; Batchelor, W.D.; Rice, M.E. Spatial Modeling of Preferred Wireworm (Coleoptera: Elateridae) Habitat. Environ. Entomol. 1998, 27, 184–190. [Google Scholar] [CrossRef]
- Furlan, L.; Contiero, B.; Chiarini, F.; Colauzzi, M.; Sartori, E.; Benvegnù, I.; Fracasso, F.; Giandon, P. Risk Assessment of Maize Damage by Wireworms (Coleoptera: Elateridae) as the First Step in Implementing IPM and in Reducing the Environmental Impact of Soil Insecticides. Environ. Sci. Pollut. Res. 2017, 24, 236–251. [Google Scholar] [CrossRef] [Green Version]
- Kozina, A.; Lemic, D.; Bazok, R.; Mikac, K.M.; Mclean, C.M.; Ivezić, M.; Igrc Barčić, J. Climatic, Edaphic Factors and Cropping History Help Predict Click Beetle (Coleoptera: Elateridae) (Agriotes Spp.) Abundance. J. Insect Sci. 2015, 15, 100. [Google Scholar] [CrossRef]
- Poggi, S.; Le Cointe, R.; Riou, J.-B.; Larroudé, P.; Thibord, J.-B.; Plantegenest, M. Relative Influence of Climate and Agroenvironmental Factors on Wireworm Damage Risk in Maize Crops. J. Pest. Sci. 2018, 91, 585–599. [Google Scholar] [CrossRef]
- Blackshaw, R.P.; Vernon, R.S. Spatial Relationships between Two Agriotes Click-Beetle Species and Wireworms in Agricultural Fields. Agric. For. Entomol. 2008, 10, 1–11. [Google Scholar] [CrossRef]
- Rawlins, R. Biology and Control of the Wheat Wireworm, Agriotes Mancus Say. Cornell Univ. Agric. Exp. Stn. Bull. 1940, 783, 1–34. [Google Scholar]
- Blackshaw, R.P.; Hicks, H. Distribution of Adult Stages of Soil Insect Pests across an Agricultural Landscape. J. Pest. Sci. 2013, 86, 53–62. [Google Scholar] [CrossRef]
- Blackshaw, R.P.; Vernon, R.S. Spatiotemporal Stability of Two Beetle Populations in Non-Farmed Habitats in an Agricultural Landscape: Agriotes Distribution in an Agricultural Landscape. J. Appl. Ecol. 2006, 43, 680–689. [Google Scholar] [CrossRef]
- Salt, G.; Hollick, F.S.J. Studies of Wireworm Populations: II. Spatial Distribution. J. Exp. Biol. 1946, 23, 1–46. [Google Scholar] [CrossRef]
- Parker, W.E.; Seeney, F.M. An Investigation into the Use of Multiple Site Characteristics to Predict the Presence and Infestation Level of Wireworms (Agriotes Sup., Coleoptera: Elateridae) in Individual Grass Fields. Ann. Appl. Biol. 1997, 130, 409–425. [Google Scholar] [CrossRef]
- Parker, W.E.; Howard, J.J. The Biology and Management of Wireworms (Agriotes Spp.) on Potato with Particular Reference to the U.K. Agric. For. Entomol. 2001, 3, 85–98. [Google Scholar] [CrossRef]
- Blackshaw, R.P.; Vernon, R.S.; Thiebaud, F. Large Scale Agriotes Spp. Click Beetle (Coleoptera: Elateridae) Invasion of Crop Land from Field Margin Reservoirs: Click Beetle Dispersal. Agric. For. Entomol. 2017. [Google Scholar] [CrossRef]
- Poggi, S.; Sergent, M.; Mammeri, Y.; Plantegenest, M.; Le Cointe, R.; Bourhis, Y. Dynamic Role of Grasslands as Sources of Soil-Dwelling Insect Pests: New Insights from in Silico Experiments for Pest Management Strategies. Ecol. Model. 2021, 440, 109378. [Google Scholar] [CrossRef]
- Furlan, L. IPM Thresholds for Agriotes Wireworm Species in Maize in Southern Europe. J. Pest. Sci. 2014, 87. [Google Scholar] [CrossRef] [Green Version]
- Esser, A.D.; Milosavljević, I.; Crowder, D.W. Effects of Neonicotinoids and Crop Rotation for Managing Wireworms in Wheat Crops. J. Econ. Entomol. 2015, 108, 1786–1794. [Google Scholar] [CrossRef]
- Rambousek, F. Über Die Felddrahtwürmer. I. Systematischer Teil. Z. Zuckerind. Cechoslov. Repub. 1928, 52, 393–402. [Google Scholar]
- Schaerffenberg, B. Bestimmungsschlüssel der landwirtschaftlich wichtigsten Drahtwürmer. Anz. Für Schädlingskunde 1940, 16, 90–96. [Google Scholar] [CrossRef]
- Pic, M.; Pierre, E.; Martinez, M.; Genson, G.; Rasplus, J.-Y.; Albert, H. Wireworms of genus Agriotes uncovered from their genetic prints. In Proceedings of the 9th Conférence Internationale sur les Ravageurs en Agriculture, Montpellier, France, 22 October 2008. [Google Scholar]
- Staudacher, K.; Pitterl, P.; Furlan, L.; Cate, P.C.; Traugott, M. PCR-Based Species Identification of Agriotes Larvae. Bull. Entomol. Res. 2011, 101, 201–210. [Google Scholar] [CrossRef]
- Heimbach, U.; Lehmhus, J.; Zamani-Noor, N. Clarification of Efficacy Data Requirements for the Authorization of an Insecticideapplied as Seed Treatment for the Control of Wireworms Incrops Such Asmaize, Sunflowers, Millet and Sugar Beet in the EU; European and Mediterranean Plant Protection Organization (EPPO): Paris, France, 2020. [Google Scholar]
- Lehmhus, J. Wireworm Biology in Middle Europe—What Are We Facing? Microbial and Nematode Control of Invertebrate Pests. IOBC-WPRS Bull. 2020, 150, 96–99. [Google Scholar]
- Eidt, D.C. A Description of the Larva of Agriotes Mancus (Say), with a Key Separating the Larvae of A. Lineatus (L.), A. Mancus, A. Obscurus (L.), and A. Sputator (L.) from Nova Scotia. Can. Entomol 1954, 86, 481–494. [Google Scholar] [CrossRef]
- Benefer, C.M.; van Herk, W.G.; Ellis, J.S.; Blackshaw, R.P.; Vernon, R.S.; Knight, M.E. The Molecular Identification and Genetic Diversity of Economically Important Wireworm Species (Coleoptera: Elateridae) in Canada. J. Pest. Sci. 2013, 86, 19–27. [Google Scholar] [CrossRef]
- Glen, R.; King, K.M.; Arnason, A.P. The Identification of Wireworms of Economic Importance in Canada. Can. J. Res. 1943, 21d, 358–387. [Google Scholar] [CrossRef]
- Riley, T.J.; Keaster, A.J. Wireworms Associated with Corn: Identification of Larvae of Nine Species of Melanotus1 from the North Central States2. Ann. Entomol. Soc. Am. 1979, 72, 408–414. [Google Scholar] [CrossRef]
- Etzler, F.E.; Wanner, K.W.; Morales-Rodriguez, A.; Ivie, M.A. DNA Barcoding to Improve the Species-Level Management of Wireworms (Coleoptera: Elateridae). J. Econ. Entomol 2014, 107, 1476–1485. [Google Scholar] [CrossRef]
- Oba, Y.; Ôhira, H.; Murase, Y.; Moriyama, A.; Kumazawa, Y. DNA Barcoding of Japanese Click Beetles (Coleoptera, Elateridae). PLoS ONE 2015, 10, e0116612. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Liu, Y.; Shu, J.; Zhang, W.; Zhang, Y.; Wang, H. DNA Barcoding Identification and Genetic Diversity of Bamboo Shoot Wireworms (Coleoptera: Elateridae) in South China. J. Asia Pac. Entomol. 2019, 22, 140–150. [Google Scholar] [CrossRef]
- Milosavljević, I.; Esser, A.D.; Crowder, D.W. Seasonal Population Dynamics of Wireworms in Wheat Crops in the Pacific Northwestern United States. J. Pest. Sci. 2017, 90, 77–86. [Google Scholar] [CrossRef]
- Staudacher, K.; Schallhart, N.; Pitterl, P.; Wallinger, C.; Brunner, N.; Landl, M.; Kromp, B.; Glauninger, J.; Traugott, M. Occurrence of Agriotes Wireworms in Austrian Agricultural Land. J. Pest. Sci. 2013, 86, 33–39. [Google Scholar] [CrossRef] [Green Version]
- Saussure, S.; Plantegenest, M.; Thibord, J.-B.; Larroudé, P.; Poggi, S. Management of Wireworm Damage in Maize Fields Using New, Landscape-Scale Strategies. Agron. Sustain. Dev. 2015, 35, 793–802. [Google Scholar] [CrossRef] [Green Version]
- Milosavljević, I.; Esser, A.D.; Crowder, D.W. Effects of Environmental and Agronomic Factors on Soil-Dwelling Pest Communities in Cereal Crops. Agric. Ecosyst. Environ. 2016, 225, 192–198. [Google Scholar] [CrossRef]
- Seal, D.R.; Chalfant, R.B.; Hall, M.R. Effects of Cultural Practices and Rotational Crops on Abundance of Wireworms (Coleoptera: Elateridae) Affecting Sweet potato in Georgia. Environ. Entomol. 1992, 21, 969–974. [Google Scholar] [CrossRef]
- Salt, G.; Hollick, F.S.J. Studies of Wireworm Population: III. Some Effects of Cultivation. Ann. Appl. Biol. 1949, 36, 169–186. [Google Scholar] [CrossRef]
- Hermann, A.; Brunner, N.; Hann, P.; Wrbka, T.; Kromp, B. Correlations between Wireworm Damages in Potato Fields and Landscape Structure at Different Scales. J. Pest. Sci. 2013, 86, 41–51. [Google Scholar] [CrossRef]
- Furlan, L.; Contiero, B.; Chiarini, F.; Benvegnù, I.; Tóth, M. The Use of Click Beetle Pheromone Traps to Optimize the Risk Assessment of Wireworm (Coleoptera: Elateridae) Maize Damage. Sci. Rep. 2020, 10, 8780. [Google Scholar] [CrossRef]
- Furlan, L.; Vasileiadis, V.P.; Chiarini, F.; Huiting, H.; Leskovšek, R.; Razinger, J.; Holb, I.J.; Sartori, E.; Urek, G.; Verschwele, A.; et al. Risk Assessment of Soil-Pest Damage to Grain Maize in Europe within the Framework of Integrated Pest Management. Crop. Prot. 2017, 97, 52–59. [Google Scholar] [CrossRef]
- Saguez, J.; Latraverse, A.; De Almeida, J.; van Herk, W.G.; Vernon, R.S.; Légaré, J.-P.; Moisan-De Serres, J.; Fréchette, M.; Labrie, G. Wireworm in Quebec Field Crops: Specific Community Composition in North America. Environ. Entomol. 2017, 46, 814–825. [Google Scholar] [CrossRef]
- Butler, L.I.; McDonough, L.M.; Onsager, J.A.; Landis, B.J. Sex Pheromones of the Pacific Coast Wireworm, Limonius Canus 12. Environ. Entomol. 1975, 4, 229–230. [Google Scholar] [CrossRef]
- Jacobson, M.; Lilly, C.E.; Harding, C. Sex Attractant of Sugar Beet Wireworm: Identification and Biological Activity. Science 1968, 159, 208–210. [Google Scholar] [CrossRef]
- 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 (Col., Elateridae). J. Appl. Entomol. 1996, 120, 463–466. [Google Scholar] [CrossRef]
- Borg-Karlson, A.-K.; Ågren, L.; Dobson, H.; Bergström, G. Identification and Electroantennographic Activity of Sex-Specific Geranyl Esters in an Abdominal Gland of FemaleAgriotes Obscurus (L.) AndA. Lineatus (L.) (Coleoptera, Elateridae). Experientia 1988, 44, 531–534. [Google Scholar] [CrossRef]
- Tóth, M.; Furlan, L.; Yatsynin, V.G.; Ujváry, I.; Szarukán, 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: Pheromones and Optimization of Bait Composition for Click Beetles. Pest. Manag. Sci. 2003, 59, 417–425. [Google Scholar] [CrossRef]
- Burgio, G.; Ragaglini, G.; Petacchi, R.; Ferrari, R.; Pozzati, M.; Furlan, L. Optimization of Agriotes Sordidus Monitoring in Northern Italy Rural Landscape, Using a Spatial Approach. Bull. Insectol. 2012, 65, 123–131. [Google Scholar]
- Vernon, R.S. A Ground-Based Pheromone Trap for Monitoring Agriotes Lineatus and A. Obscurus (Coleoptera: Elateridae). J. Entomol. Soc. Br. Columbia 2004, 101, 141–142. [Google Scholar]
- Witzgall, P.; Kirsch, P.; Cork, A. Sex Pheromones and Their Impact on Pest Management. J. Chem. Ecol. 2010, 36, 80–100. [Google Scholar] [CrossRef] [PubMed]
- Blackshaw, R.P.; van Herk, W.G.; Vernon, R.S. Determination of Agriotes Obscurus (Coleoptera: Elateridae) Sex Pheromone Attraction Range Using Target Male Behavioural Responses: Pheromone Attraction Range of Agriotes Obscurus. Agr For. Entomol. 2018, 20, 228–233. [Google Scholar] [CrossRef]
- Sufyan, M.; Neuhoff, D.; Furlan, L. Assessment of the Range of Attraction of Pheromone Traps to Agriotes Lineatus and Agriotes Obscurus. Agric. For. Entomol. 2011, 13, 313–319. [Google Scholar] [CrossRef]
- Hicks, H.; Blackshaw, R.P. Differential Responses of Three Agriotes Click Beetle Species to Pheromone Traps. Agric. For. Entomol. 2008, 10, 443–448. [Google Scholar] [CrossRef]
- Kishita, M.; Arakaki, N.; Kawamura, F.; Sadoyama, Y.; Yamamura, K. Estimation of Population Density and Dispersal Parameters of the Adult Sugarcane Wireworm, Melanotus Okinawensis Ohira (Coleoptera: Elateridae), on Ikei Island, Okinawa, by Mark-Recapture Experiments. Appl. Entomol. Zool. 2003, 38, 233–240. [Google Scholar] [CrossRef] [Green Version]
- Benefer, C.M.; Knight, M.E.; Ellis, J.S.; Hicks, H.; Blackshaw, R.P. Understanding the Relationship between Adult and Larval Agriotes Distributions: The Effect of Sampling Method, Species Identification and Abiotic Variables. Appl. Soil Ecol. 2012, 53, 39–48. [Google Scholar] [CrossRef]
- Reddy, G.V.P.; Tangtrakulwanich, K. Potential Application of Pheromones in Monitoring, Mating Disruption, and Control of Click Beetles (Coleoptera: Elateridae). ISRN Entomol. 2014, 2014, 1–8. [Google Scholar] [CrossRef] [Green Version]
- 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 1975, 107, 1233–1252. [Google Scholar] [CrossRef]
- Doane, J.F.; Klingler, J. Location of Co2-Receptive Sensilla on Larvae of the Wireworms Agriotes Lineatus-Obscurus and Limonius Californicus1. Ann. Entomol. Soc. Am. 1978, 71, 357–363. [Google Scholar] [CrossRef]
- Parker, W.E. Evaluation of the Use of Food Baits for Detecting Wireworms (Agriotes Spp., Coleoptera: Elateridae) in Fields Intended for Arable Crop Production. Crop. Prot. 1994, 13, 271–276. [Google Scholar] [CrossRef]
- Brunner, N.; Grünbacher, E.M.; Kromp, B. Comparison of Three Different Bait Trap Types for Wireworms (Coleoptera: Elateridae) in Arable Crops. IOBS/WPRS Bull. 2007, 30, 47–52. [Google Scholar]
- Morales-Rodriguez, A.; Ospina, A.; Wanner, K.W. Evaluation of Four Bait Traps for Sampling Wireworm (Coleoptera: Elateridae) Infesting Cereal Crops in Montana. Int. J. Insect Sci. 2017, 9, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Landl, M.; Furlan, L.; Glauninger, J. Seasonal Fluctuations in Agriotes Spp. (Coleoptera: Elateridae) at Two Sites in Austria and the Efficiency of Bait Trap Designs for Monitoring Wireworm Populations in the Soil. J. Plant. Dis. Prot. 2010, 117, 268–272. [Google Scholar] [CrossRef]
- Chabert, A.; Blot, Y. Estimation Des Populations Larvaires de Taupins Par Un Piège Attractif. Phytoma 1992, 436, 26–30. [Google Scholar]
- Kirfman, G.W.; Keaster, A.J.; Story, R.N. An Improved Wireworm (Coleoptera: Elateridae) Sampling Technique for Midwest Cornfields. J. Kans. Entomol Soc. 1986, 59, 37–41. [Google Scholar]
- Cherry, R.; Grose, P.; Barbieri, E. Validation of a Sequential Sampling Plan for Wireworms (Coleoptera: Elateridae) at Sugarcane Planting. J. Pest. Sci. 2013, 86, 29–32. [Google Scholar] [CrossRef]
- Griffiths, D.C. Susceptibility of Plants to Attack by Wireworms (Agriotes Spp.). Ann. Appl. Biol. 1974, 78, 7–13. [Google Scholar] [CrossRef]
- Milosavljević, I.; Esser, A.D.; Murphy, K.M.; Crowder, D.W. Effects of Imidacloprid Seed Treatments on Crop Yields and Economic Returns of Cereal Crops. Crop. Prot. 2019, 119, 166–171. [Google Scholar] [CrossRef]
- Furlan, L.; Bonetto, C.; Finotto, A.; Lazzeri, L.; Malaguti, L.; Patalano, G.; Parker, W. The Efficacy of Biofumigant Meals and Plants to Control Wireworm Populations. Ind. Crop. Prod. 2010, 31, 245–254. [Google Scholar] [CrossRef]
- Furlan, L.; Bonetto, C.; Costa, B.; Finotto, A.; Lazzeri, L. Observations on Natural Mortality Factors in Wireworm Populations and Evaluation of Management Options. IOBC/WPRS Bull. 2009, 45, 436–439. [Google Scholar]
- Lees, A.D. On the Behaviour of Wireworms of the Genus Agriotes Esch. (Coleoptera, Elateridae). J. Exp. Biol. 1943, 20, 54–60. [Google Scholar] [CrossRef]
- Landis, B.J.; Onsager, J.A. Wireworms on Irrigated Lands in the West: How to Control Them. In Farmer’s Bulletin; U.S. Department of Agriculture: Washington, DC, USA, 1966. [Google Scholar]
- Shirck, F.H. Crop Rotations and Cultural Practices as Related to Wireworm Control in Idaho12. J. Econ. Entomol. 1945, 38, 627–633. [Google Scholar] [CrossRef]
- Hall, D.G.; Cherry, R.H. Effect of Temperature in Flooding to Control the Wireworm Melanotus Communis (Coleoptera: Elateridae). Fla. Entomol. 1993, 76, 155. [Google Scholar] [CrossRef]
- Van Herk, W.G.; Vernon, R.S. Effect of Temperature and Soil on the Control of a Wireworm, Agriotes Obscurus L. (Coleoptera: Elateridae) by Flooding. Crop. Prot. 2006, 25, 1057–1061. [Google Scholar] [CrossRef]
- Onsager, J.A.; Foiles, L.L. Chemical Control of the Great Basin Wireworm on Potatoes. J. Econ. Entomol. 1969, 62, 1506–1507. [Google Scholar] [CrossRef]
- Andrews, N.; Ambrosino, M.; Fisher, G.; Rondon, S.I. Wireworm Biology and Nonchemical Management in Potatoes in the Pacific Northwest; A Pacific Northwest Extension Publication, Oregon State University: Corvallis, OR, USA, 2008. [Google Scholar]
- Samoylova, E.S.; Tiunov, A.V. Flexible Trophic Position of Polyphagous Wireworms (Coleoptera, Elateridae): A Stable Isotope Study in the Steppe Belt of Russia. Appl. Soil Ecol. 2017, 121, 74–81. [Google Scholar] [CrossRef]
- Lane, M.C.; Jones, E.W. Flooding As A Means of Reducing Wireworm Infestations. J. Econ. Entomol. 1936, 29, 842–850. [Google Scholar] [CrossRef]
- Genung, W.G. Flooding Experiments for Control of Wireworms Attacking Vegetable Crops in the Everglades. Fla. Entomol. 1970, 53, 55. [Google Scholar] [CrossRef]
- Arakaki, N.; Nagayama, A.; Kobayashi, A.; Kishita, M.; Sadoyama, Y.; Mougi, N.; Kawamura, F.; Wakamura, S.; Yamamura, K. Control of the Sugarcane Click Beetle Melanotus Okinawensis Ohira (Coleoptera: Elateridae) by Mass Trapping Using Synthetic Sex Pheromone on Ikei Island, Okinawa, Japan. Appl. Entomol. Zool. 2008, 43, 37–47. [Google Scholar] [CrossRef] [Green Version]
- Arakaki, N.; Nagayama, A.; Kobayashi, A.; Tarora, K.; Kishita, M.; Sadoyama, Y.; Mougi, N.; Kijima, K.; Suzuki, Y.; Akino, T.; et al. Estimation of Abundance and Dispersal Distance of the Sugarcane Click Beetle Melanotus Sakishimensis Ohira (Coleoptera: Elateridae) on Kurima Island, Okinawa, by Mark-Recapture Experiments. Appl. Entomol. Zool. 2008, 43, 409–419. [Google Scholar] [CrossRef] [Green Version]
- Sufyan, M.; Neuhoff, D.; Furlan, L. Effect of Male Mass Trapping of Agriotes Species on Wireworm Abundance and Potato Tuber Damage. Bull. Insectol. 2013, 66, 135–142. [Google Scholar]
- Vernon, R.S.; Blackshaw, R.P.; van Herk, W.G.; Clodius, M. Mass Trapping Wild Agriotes Obscurus and Agriotes Lineatus Males with Pheromone Traps in a Permanent Grassland Population Reservoir: Pheromone Trapping of Agriotes Beetles. Agr For. Entomol. 2014, 16, 227–239. [Google Scholar] [CrossRef]
- Ritter, C.; Richter, E. Control Methods and Monitoring of Agriotes Wireworms (Coleoptera: Elateridae). J. Plant. Dis. Prot. 2013, 120, 4–15. [Google Scholar] [CrossRef]
- Van Herk, W.G.; Vernon, R.S. Local Depletion of Click Beetle Populations by Pheromone Traps Is Weather and Species Dependent. Environ. Entomol. 2020, 49, 449–460. [Google Scholar] [CrossRef]
- Van Lenteren, J.C.; Bolckmans, K.; Köhl, J.; Ravensberg, W.J.; Urbaneja, A. Biological Control Using Invertebrates and Microorganisms: Plenty of New Opportunities. BioControl 2018, 63, 39–59. [Google Scholar] [CrossRef] [Green Version]
- 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 2013, 86, 99–106. [Google Scholar] [CrossRef]
- Hyslop, J.A. Wireworms Attacking Cereal and Forage Crops; U.S. Dept. of Agriculture: Washington, DC, USA, 1915. [Google Scholar]
- Subklew, W. Die Bekämpfung Der Elateriden: Eine Übersicht Über Die Literatur. Z. Für Angew. Entomol. 1938, 24, 511–581. [Google Scholar] [CrossRef]
- Kirk, D.A.; Evenden, M.D.; Mineau, P. Past and Current Attempts to Evaluate the Role of Birds as Predators of Insect Pests in Temperate Agriculture. In Current Ornithology; Nolan, V., Ketterson, E.D., Eds.; Springer: Boston, MA, USA, 1996; pp. 175–269. ISBN 978-1-4613-7697-2. [Google Scholar]
- 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 1956, 88, 228–231. [Google Scholar] [CrossRef]
- 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. 2015, 139, 154–157. [Google Scholar] [CrossRef]
- Rabb, R.L. Biology of Conoderus Vespertinus in the Piedmont Section of North Carolina (Coleoptera: Elateridae). Ann. Entomol. Soc. Am. 1963, 56, 669–676. [Google Scholar] [CrossRef]
- Rizzo, C.; Lehmhus, J. Wireworm Food Choice: Steack or Salad? Jul. Kühn Arch. 2014, 447, 543–544. [Google Scholar]
- Traugott, M.; Schallhart, N.; Kaufmann, R.; Juen, A. The Feeding Ecology of Elaterid Larvae in Central European Arable Land: New Perspectives Based on Naturally Occurring Stable Isotopes. Soil Biol. Biochem. 2008, 40, 342–349. [Google Scholar] [CrossRef]
- D’Aguilar, J. Sur Paracodrus Apterogynus Hal. (Hym. Proctotrupidae), Parasite Des Larves d’Agriotes En France. Bull. Soc. Entomol. Fr. 1948, 53, 154–155. [Google Scholar]
- Langenbuch, R. Beiträge Zur Kenntnis Der Biologie von Agriotes Lineatus L. Und Agriotes Obscurus L. Z. Für Angew. Entomol. 1932, 19, 278–300. [Google Scholar] [CrossRef]
- Leclerque, A.; Kleespies, R.G.; Ritter, C.; Schuster, C.; Feiertag, S. Genetic and Electron-Microscopic Characterization of ‘Rickettsiella Agriotidis’, a New Rickettsiella Pathotype Associated with Wireworm, Agriotes Sp. (Coleoptera: Elateridae). Curr. Microbiol. 2011, 63, 158–163. [Google Scholar] [CrossRef]
- Danismazoglu, M.; Demir, İ.; 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. 2012, 40, 1–7. [Google Scholar] [CrossRef]
- Subklew, W. Agriotes Lineatus L. Und Agriotes Obscurus L: (Ein Beitrag Zu Ihrer Morphologie Und Biologie.). Z. Für Angew. Entomol. 1935, 21, 96–122. [Google Scholar] [CrossRef]
- Zolk, K. Paracodrus Apterogynus Halid. Kui tumeda viljanaksuri (Agriotes Obscurus L.) toukude uus parasiit. Tartu Ülikooli Entomoloogia Katsejaama Teadaanded 1924, 3, 10. [Google Scholar]
- Blunck, H. Parasiten Der Elateridenlarven. Z. Für Angew. Entomol. 1925, 11, 148–149. [Google Scholar] [CrossRef]
- Nixon, G.E.J. A Preliminary Revision of the British Proctotrupinae (Hym., Proctotrupoidea). Trans. R. Entomol. Soc. Lond. 1938, 87, 431–465. [Google Scholar] [CrossRef]
- Bognar, S. Pristocera Depressa a Paralysing and Destructive Parasite of the Wireworm, A. Obscurus. Novenytermeles 1955, 4, 241–252. [Google Scholar]
- Kabaluk, J.T.; Goettel, M.; Erlandson, M.; Ericsson, J.; Duke, G.M.; Vernon, R.S. Metarhizium Anisopliae as a Biological Control for Wireworms and a Report of Some Other Naturally-Occurring Parasites. IOBC/WPRS Bull. 2005, 28, 109–115. [Google Scholar]
- Nickle, W.R. A Contribution to Our Knowledge of the Mermithidae (Nematoda). J. Nematol. 1972, 4, 113–146. [Google Scholar]
- Platzer, E.G. Biological Control of Mosquitoes with Mermithids. J. Nematol. 1981, 13, 257–262. [Google Scholar] [PubMed]
- Doane, J.F.; Klingler, J.; Welch, H.E. Parasitism of Agriotes Obscurus Linnaeus (Coleoptera: Elateridae) by Hexamermis Sp. (Nematoda: Mermithidae. B. Soc. Entomol. Suisse 1973, 45, 299–300. [Google Scholar]
- Stock, S.P.; Blair, H.G. Entomopathogenic Nematodes and Their Bacterial Symbionts: The inside out of a Mutualistic Association. Symbiosis 2008, 46, 65–75. [Google Scholar]
- 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. 2009, 100, 100–105. [Google Scholar] [CrossRef]
- Eidt, D.C.; Thurston, G.S. Physical Deterrents to Infection by Entomopathogenic Nematodes in Wireworms (Coleoptera: Elateridae) and Other Soil Insects. Can. Entomol. 1995, 127, 423–429. [Google Scholar] [CrossRef]
- 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. 1983, 15, 597–601. [Google Scholar]
- 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. JASHS 1993, 118, 605–608. [Google Scholar] [CrossRef]
- Kovacs, A.; Deseo, K.V.; Poinar, J.G.O.; De Leoardis, A. Prove Di Lotta Contro Insetti Con Applicazione Di Nematode Entomogeni. ATTI G Fitopatol. 1980, 1, 499–546. [Google Scholar]
- Ansari, M.A.; Evans, M.; Butt, T.M. Identification of Pathogenic Strains of Entomopathogenic Nematodes and Fungi for Wireworm Control. Crop. Prot. 2009, 28, 269–272. [Google Scholar] [CrossRef]
- Ester, A.; Huiting, H. Controlling Wireworms (Agriotes Spp.) in a Potato Crop with Biologicals. IOBC/WPRS Bull. 2007, 30, 189–196. [Google Scholar]
- Rahatkhah, Z.; Karimi, J.; Ghadamyari, M.; Brivio, M.F. Immune Defenses of Agriotes Lineatus Larvae against Entomopathogenic Nematodes. BioControl 2015, 60, 641–653. [Google Scholar] [CrossRef]
- Morton, A.; Garcia-del-Pino, F. Laboratory and Field Evaluation of Entomopathogenic Nematodes for Control of Agriotes Obscurus (L.) (Coleoptera: Elateridae). J. Appl. Entomol. 2017, 141, 241–246. [Google Scholar] [CrossRef]
- Turian, G. Entomophthora Elateridiphaga n.Sp. Sur Imagos d’Agriotes Sputator L. Bull. Soc. Entomol. Suisse 1978, 51, 395–398. [Google Scholar]
- Keller, S. The Fungus Zoophthora Elateridiphaga as an Important Mortality Factor of the Click Beetle Agriotes Sputator. J. Invertebr. Pathol. 1994, 63, 90–91. [Google Scholar] [CrossRef]
- Dara, S.K.; Humber, R.A. Entomophthoran. In Beneficial Microbes in Agro-Ecology; Elsevier: Amsterdam, The Netherlands, 2020; pp. 757–775. ISBN 978-0-12-823414-3. [Google Scholar]
- Keller, S. Zoophthora Elateridiphaga (Zygomycetes, Entomophthoraceae) Causing Epizootics in Populations of Notostira Elongata (Heteroptera, Miridae). Bull. Soc. Entomol. Suisse 1982, 55, 289–296. [Google Scholar]
- McCoy, C.W. Entomogenous Fungi as Microbial Pesticides. In Proceedings of the New Directions in Biological Control. Alternatives for Suppressing Agricultural Pests and Diseases; Baker, R.R., Dunn, P.E., Eds.; Wiley: New York, NY, USA, 1990. [Google Scholar]
- 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. 1973, 21, 101–106. [Google Scholar] [CrossRef]
- Leger, R.J.S.; Goettel, M.; Roberts, D.W.; Staples, R.C. Prepenetration Events during Infection of Host Cuticle by Metarhizium Anisopliae. J. Invertebr. Pathol. 1991, 58, 168–179. [Google Scholar] [CrossRef]
- Ladurner, E.; Quentin, U.; Franceschini, S.; Benuzzi, M. Efficacy Evaluation of the Entomopathogenic Fungus Beauveria Bassiana Strain ATCC 74040 against Wireworms (Agriotes Spp.) on Potato. IOBC/WPRS Bull. 2009, 45, 445–448. [Google Scholar]
- Schepl, U.; Paffrath, A.; Kempkens, K. Regulierungskonzepte Zur Reduktion von Drahtwurmschäden; Landwirtschaftskammer Nordrhein-Westfalen: Münster, Germany, 2010; 55p. [Google Scholar]
- Kölliker-Ott, U.; Biasio, L.; Jossi, W. Potential Control of Swiss Wireworms with Entomopathogenic Fungi. IOBC/WPRS BULL. 2011, 66, 517–520. [Google Scholar]
- Eckard, S.; Ansari, M.A.; Bacher, S.; Butt, T.M.; Enkerli, J.; Grabenweger, G. Virulence of in Vivo and in Vitro Produced Conidia of Metarhizium Brunneum Strains for Control of Wireworms. Crop. Prot. 2014, 64, 137–142. [Google Scholar] [CrossRef]
- Zacharuk, R.Y.; Tinline, R.D. Pathogenicity of Metarrhizium Anisopliae, and Other Fungi, for Five Elaterids (Coleoptera) in Saskatchewan. J. Invertebr. Pathol. 1968, 12, 294–309. [Google Scholar] [CrossRef]
- Kabaluk, T.; Li-Leger, E.; Nam, S. Metarhizium Brunneum—An Enzootic Wireworm Disease and Evidence for Its Suppression by Bacterial Symbionts. J. Invertebr. Pathol. 2017, 150, 82–87. [Google Scholar] [CrossRef]
- Gillespie, A.T.; Claydon, N. The Use of Entomogenous Fungi for Pest Control and the Role of Toxins in Pathogenesis. Pestic. Sci. 1989, 27, 203–215. [Google Scholar] [CrossRef]
- Rogge, S.A.; Mayerhofer, J.; Enkerli, J.; Bacher, S.; Grabenweger, G. Preventive Application of an Entomopathogenic Fungus in Cover Crops for Wireworm Control. BioControl 2017, 62, 613–623. [Google Scholar] [CrossRef] [Green Version]
- Kabaluk, J.T.; Ericsson, J.D. Environmental and Behavioral Constraints on the Infection of Wireworms by Metarhizium Anisopliae. Environ. Entomol. 2007, 36, 1415–1420. [Google Scholar] [CrossRef]
- Brian, M.V. On the Ecology of Beetles of the Genus Agriotes with Special Reference to A. Obscurus. J. Anim. Ecol. 1947, 16, 210. [Google Scholar] [CrossRef]
- Burrage, R.H. Seasonal Feeding of Larvae of Ctenicera Destructor and Hypolithus Bicolor (Coleoptera: Elateridae) on Potatoes Placed in the Field at Weekly Intervals. Ann. Entomol. Soc. Am. 1963, 56, 306–313. [Google Scholar] [CrossRef]
- Sonnemann, I.; Grunz, S.; Wurst, S. Horizontal Migration of Click Beetle (Agriotes Spp.) Larvae Depends on Food Availability. Entomol. Exp. Appl. 2014, 150, 174–178. [Google Scholar] [CrossRef]
- Staley, J.T.; Hodgson, C.J.; Mortimer, S.R.; Morecroft, M.D.; Masters, G.J.; Brown, V.K.; Taylor, M.E. Effects of Summer Rainfall Manipulations on the Abundance and Vertical Distribution of Herbivorous Soil Macro-Invertebrates. Eur. J. Soil Biol. 2007, 43, 189–198. [Google Scholar] [CrossRef]
- Vänninen, I. Distribution and Occurrence of Four Entomopathogenic Fungi in Finland: Effect of Geographical Location, Habitat Type and Soil Type. Mycol. Res. 1996, 100, 93–101. [Google Scholar] [CrossRef]
- Rohde, C.; Moino, A., Jr.; da Silva, M.A.T.; Carvalho, F.D.; Ferreira, C.S. Influence of Soil Temperature and Moisture on the Infectivity of Entomopathogenic Nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) against Larvae of Ceratitis Capitata (Wiedemann) (Diptera: Tephritidae). Neotrop. Entomol. 2010, 39, 608–611. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Khoury, Y.; Oreste, M.; Noujeim, E.; Nemer, N.; Tarasco, E. Effect of Temperature on the Pathogenecity of Mediterranean Native Entomopathogenic Nematodes (Steinernematidae and Heterorhabditidae) from Natural Ecosystems. Redia 2018, 123–127. [Google Scholar] [CrossRef]
- Ensafi, P.; Crowder, D.W.; Esser, A.D.; Zhao, Z.; Marshall, J.M.; Rashed, A. Soil Type Mediates the Effectiveness of Biological Control Against Limonius Californicus (Coleoptera: Elateridae). J. Econ. Entomol. 2018, 111, 2053–2058. [Google Scholar] [CrossRef]
- El-Borai, F.E.; Stuart, R.J.; Campos-Herrera, R.; Pathak, E.; Duncan, L.W. Entomopathogenic Nematodes, Root Weevil Larvae, and Dynamic Interactions among Soil Texture, Plant Growth, Herbivory, and Predation. J. Invertebr. Pathol. 2012, 109, 134–142. [Google Scholar] [CrossRef] [Green Version]
- Toledo, J.; Williams, T.; Pérez, C.; Liedo, P.; Valle, J.F.; Ibarra, J.E. Abiotic Factors Affecting the Infectivity of Steinernema Carpocapsae (Rhabditida: Steinernematidae) on Larvae of Anastrepha Obliqua (Diptera: Tephritidae). Biocontrol. Sci. Technol. 2009, 19, 887–898. [Google Scholar] [CrossRef]
- Toepfer, S.; Kurtz, B.; Kuhlmann, U. Influence of Soil on the Efficacy of Entomopathogenic Nematodes in Reducing Diabrotica Virgifera Virgifera in Maize. J. Pest. Sci. 2010, 83, 257–264. [Google Scholar] [CrossRef] [Green Version]
- 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. 2007, 100, 31–38. [Google Scholar] [CrossRef]
- Glare, T.R. Stage-dependent Synergism Using Metarhizium Anisopliae and Serratia Entomophila against Costelytra Zealandica. Biocontrol. Sci. Technol. 1994, 4, 321–329. [Google Scholar] [CrossRef]
- Ansari, M.A.; Shah, F.A.; Butt, T.M. Combined Use of Entomopathogenic Nematodes and Metarhizium Anisopliae as a New Approach for Black Vine Weevil, Otiorhynchus Sulcatus, Control. Entomol. Exp. Appl. 2008, 129, 340–347. [Google Scholar] [CrossRef]
- Dlamini, B.E.; Malan, A.P.; Addison, P. Combined Effect of Entomopathogenic Fungi and Steinernema Yirgalemense against the Banded Fruit Weevil, Phlyctinus Callosus (Coleoptera: Curculionidae). Biocontrol. Sci. Technol. 2020, 30, 1169–1179. [Google Scholar] [CrossRef]
- Usman, M.; Gulzar, S.; Wakil, W.; Wu, S.; Piñero, J.C.; Leskey, T.C.; Nixon, L.J.; Oliveira-Hofman, C.; Toews, M.D.; Shapiro-Ilan, D. Virulence of Entomopathogenic Fungi to Rhagoletis Pomonella (Diptera: Tephritidae) and Interactions With Entomopathogenic Nematodes. J. Econ. Entomol. 2020, 113, 2627–2633. [Google Scholar] [CrossRef]
- Jaronski, S.T. Ecological Factors in the Inundative Use of Fungal Entomopathogens. BioControl 2010, 55, 159–185. [Google Scholar] [CrossRef]
- Jaronski, S.T.; Jackson, M.A. Efficacy of Metarhizium Anisopliae Microsclerotial Granules. Biocontrol Sci. Technol. 2008, 18, 849–863. [Google Scholar] [CrossRef]
- Reddy, G.V.P.; Tangtrakulwanich, K.; Wu, S.; Miller, J.H.; Ophus, V.L.; Prewett, J.; Jaronski, S.T. Evaluation of the Effectiveness of Entomopathogens for the Management of Wireworms (Coleoptera: Elateridae) on Spring Wheat. J. Invertebr. Pathol. 2014, 120, 43–49. [Google Scholar] [CrossRef] [Green Version]
- Küppers, R.; Neuhoff, D.; Stumm, C. Einfluss Des Biologischen Insektizids ATTRACAP® Auf Den Drahtwurmbefall von Speisekartoffeln. In Leitbetriebe Ökologischer Landbau Nordrhein-Westfalen; Agrarökologie & Organischer Landbau, Universität Bonn: Bonn, Germany, 2017; pp. 114–128. [Google Scholar]
- Brandl, M.A.; Schumann, M.; Przyklenk, M.; Patel, A.; Vidal, S. Wireworm Damage Reduction in Potatoes with an Attract-and-Kill Strategy Using Metarhizium Brunneum. J. Pest. Sci. 2017, 90, 479–493. [Google Scholar] [CrossRef]
- Toba, H.H.; Pike, K.S.; O’Keeffe, F.E. Carbosulfan, Fonofos, and Lindane Wheat Seed Treatments for Control of Sugarbeet Wireworm. J. Agric. Entomol. 1988, 5, 35–43. [Google Scholar]
- Kuhar, T.P.; Alvarez, J.M. Timing of Injury and Efficacy of Soil-Applied Insecticides against Wireworms on Potato in Virginia. Crop. Prot. 2008, 27, 792–798. [Google Scholar] [CrossRef]
- Vernon, R.S.; Van Herk, W.; Tolman, J.; Ortiz Saavedra, H.; Clodius, M.; Gage, B. Transitional Sublethal and Lethal Effects of Insecticides after Dermal Exposures to Five Economic Species of Wireworms (Coleoptera: Elateridae). J. Econ. Entomol. 2008, 101, 365–374. [Google Scholar] [CrossRef] [PubMed]
- Klingler, J. Über Die Bedeutung Des Kohlendioxyds Für Die Orientierung Der Larven von Otiorrhynchus Sulcatus F., Melolontha Und Agriotes (Col.) Im Boden (Vorläufige Mitteilung). Bull. Soc. Entomol. Suisse 1957, 30, 317–322. [Google Scholar]
- Schumann, M.; Patel, A.; Vidal, S. Soil Application of an Encapsulated CO2 Source and Its Potential for Management of Western Corn Rootworm Larvae. J. Econ. Entomol. 2014, 107, 230–239. [Google Scholar] [CrossRef]
- Guerenstein, P.G.; Hildebrand, J.G. Roles and Effects of Environmental Carbon Dioxide in Insect Life. Ann. Rev. Entomol. 2008, 53, 161–178. [Google Scholar] [CrossRef]
- Barsics, F.; Haubruge, E.; Francis, F.; Verheggen, F. The Role of Olfaction in Wireworms: A Review on Their Foraging Behavior and Sensory Apparatus. Biotechnol. Agron. Soc. Environ. 2014, 18, 524–535. [Google Scholar]
- Barsics, F.; Delory, B.M.; Delaplace, P.; Francis, F.; Fauconnier, M.-L.; Haubruge, É.; Verheggen, F.J. Foraging Wireworms Are Attracted to Root-Produced Volatile Aldehydes. J. Pest. Sci 2017, 90, 69–76. [Google Scholar] [CrossRef]
- Johnson, S.N.; Nielsen, U.N. Foraging in the Dark—Chemically Mediated Host Plant Location by Belowground Insect Herbivores. J. Chem. Ecol. 2012, 38, 604–614. [Google Scholar] [CrossRef]
- La Forgia, D.; Jaffuel, G.; Campos-Herrera, R.; Verheggen, F.; Turlings, T. Efficiency of an Attract-and-Kill System with Entomopathogenic Nematodes against Wireworms (Coleoptera: Elateridae). IOBC/WPRS Bull. 2020, 150, 91–95. [Google Scholar]
- 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. 2015, 88, 707–716. [Google Scholar] [CrossRef]
- Vuts, J.; Furlan, L.; Csonka, É.B.; Woodcock, C.M.; Caulfield, J.C.; Mayon, P.; Pickett, J.A.; Birkett, M.A.; Tóth, M. Development of a Female Attractant for the Click Beetle Pest Agriotes Brevis: Plant Attractants for Female Click Beetles. Pest. Manag. Sci. 2014, 70, 610–614. [Google Scholar] [CrossRef]
- Vuts, J.; Furlan, L.; Tóth, M. Female Responses to Synthetic Pheromone and Plant Compounds in Agriotes Brevis Candeze (Coleoptera: Elateridae). J. Insect Behav. 2018, 31, 106–117. [Google Scholar] [CrossRef]
- Tóth, M.; Furlan, L.; Vuts, J.; Szarukán, I.; Ujváry, I.; Yatsynin, V.G.; Tolasch, T.; Francke, W. Geranyl Hexanoate, the Female-Produced Pheromone of Agriotes Sordidus Illiger (Coleoptera: Elateridae) and Its Activity on Both Sexes. Chemoecology 2015, 25, 1–10. [Google Scholar] [CrossRef]
- Tóth, M.; Furlan, L.; Szarukán, I.; Nagy, A.; Vuts, J.; Toshova, T.; Velchev, D.; Lohonyai, Z.; Imrei, Z. The Addition of a Pheromone to a Floral Lure Increases Catches of Females of the Click Beetle Agriotes Ustulatus (Schaller) (Coleoptera: Elateridae). J. Chem. Ecol. 2019, 45, 667–672. [Google Scholar] [CrossRef] [Green Version]
- Doane, J.F. The Flat Wireworm, Aeolus Mellillus: Studies on Seasonal Occurrence of Adults and Incidence of the Larvae in the Wireworm Complex Attacking Wheat in Saskatchewan1. Environ. Entomol. 1977, 6, 818–820. [Google Scholar] [CrossRef]
- Jansson, R.K.; Seal, D.R. Biology and Management of Wireworms on Potato. In Proceedings of the International Conference on ‘Advances in Potato Pest Biology and Management’, Jackson Hole, WY, USA, 12–17 October 1991; pp. 31–53. [Google Scholar]
- Vernon, B.; Pats, P. Distribution of Two European Wireworms, Agriotes Lineatus and A. Obscurus in British Columbia. J. Entomol. Soc. Br. Columbia 1997, 94, 59–62. [Google Scholar]
- Mahéo, F.; Lehmhus, J.; Larroudé, P.; Le Cointe, R. Un Outil Moléculaire Simple et Abordable Pour Identifier Les Larves de Taupins Du Genre Agriotes. Cah. Tech. Inra 2020, 102, 1–8. [Google Scholar]
- Andrews, K.R.; Gerritsen, A.; Rashed, A.; Crowder, D.W.; Rondon, S.I.; van Herk, W.G.; Vernon, R.; Wanner, K.W.; Wilson, C.M.; New, D.D.; et al. Wireworm (Coleoptera: Elateridae) Genomic Analysis Reveals Putative Cryptic Species, Population Structure, and Adaptation to Pest Control. Commun. Biol. 2020, 3, 489. [Google Scholar] [CrossRef]
- Klausnitzer, B. Familie Elateridae. In Die Larven der Käfer Mitteleuropas; Gustav Fischer: Jena, Germany, 1994; pp. 118–189. [Google Scholar]
- Martensen, A.C.; Saura, S.; Fortin, M.-J. Spatio-Temporal Connectivity: Assessing the Amount of Reachable Habitat in Dynamic Landscapes. Methods Ecol. Evol. 2017, 8, 1253–1264. [Google Scholar] [CrossRef]
- Taylor, P.D.; Fahrig, L.; Henein, K.; Merriam, G. Connectivity Is a Vital Element of Landscape Structure. Oikos 1993, 68, 571. [Google Scholar] [CrossRef] [Green Version]
- Jonsson, M.; Wratten, S.D.; Landis, D.A.; Tompkins, J.-M.L.; Cullen, R. Habitat Manipulation to Mitigate the Impacts of Invasive Arthropod Pests. Biol. Invasions 2010, 12, 2933–2945. [Google Scholar] [CrossRef] [Green Version]
- Parisey, N.; Bourhis, Y.; Roques, L.; Soubeyrand, S.; Ricci, B.; Poggi, S. Rearranging Agricultural Landscapes towards Habitat Quality Optimisation: In Silico Application to Pest Regulation. Ecol. Complex. 2016, 113–122. [Google Scholar] [CrossRef]
- Polasky, S.; Nelson, E.; Camm, J.; Csuti, B.; Fackler, P.; Lonsdorf, E.; Montgomery, C.; White, D.; Arthur, J.; Garber-Yonts, B.; et al. Where to Put Things? Spatial Land Management to Sustain Biodiversity and Economic Returns. Biol. Conserv. 2008, 141, 1505–1524. [Google Scholar] [CrossRef] [Green Version]
- Jedlička, P.; Frouz, J. Population Dynamics of Wireworms (Coleoptera, Elateridae) in Arable Land after Abandonment. Biologia 2007, 62. [Google Scholar] [CrossRef]
- Neuhoff, D.; Christen, C.; Paffrath, A.; Schepl, U. Approaches to Wireworm Control in Organic Potato Production. IOBC/WPRS Bull. 2007, 30, 65–68. [Google Scholar]
- La Forgia, D.; Thibord, J.-B.; Larroudé, P.; Francis, F.; Lognay, G.; Verheggen, F. Linking Variety-Dependent Root Volatile Organic Compounds in Maize with Differential Infestation by Wireworms. J. Pest. Sci. 2020, 93, 605–614. [Google Scholar] [CrossRef]
- Rawlins, W.A. Some Varietal Differences in Wireworm Injury to Potatoes. Am. Potato J. 1943, 20, 156–158. [Google Scholar] [CrossRef]
- Parker, W.E.; Howard, J.J. Assessment of the Relative Susceptibility of Potato Cultivars to Damage by Wireworms (Agriotes Spp.). Tests Agrochem. Cultiv. 2000, 21, 15–16. [Google Scholar]
- Langdon, K.W.; Abney, M.R. Relative Susceptibility of Selected Potato Cultivars to Feeding by Two Wireworm Species at Two Soil Moisture Levels. Crop. Prot. 2017, 101, 24–28. [Google Scholar] [CrossRef]
- Kwon, M.; Hahm, Y.I.; Shin, K.Y.; Ahn, Y.J. Evaluation of Various Potato Cultivars for Resistance to Wireworms (Coleoptera: Elateridae). Am. J. Pot Res. 1999, 76, 317–319. [Google Scholar] [CrossRef]
- Sonnemann, I.; Baumhaker, H.; Wurst, S. Species Specific Responses of Common Grassland Plants to a Generalist Root Herbivore (Agriotes Spp. Larvae). Basic Appl. Ecol. 2012, 13, 579–586. [Google Scholar] [CrossRef]
- Johnson, S.N.; Gregory, P.J. Chemically-Mediated Host-Plant Location and Selection by Root-Feeding Insects. Physiol. Entomol. 2006, 31, 1–13. [Google Scholar] [CrossRef]
- La Forgia, D.; Verheggen, F. The Law of Attraction: Identification of Volatiles Organic Compounds Emitted by Potatoes as Wireworms Attractant. Commun. Agric. Appl. Biol. Sci. 2017, 82, 167–169. [Google Scholar]
- Thorpe, W.H.; Crombie, A.C.; Hill, R.; Darrah, J.H. The Behaviour of Wireworms in Response to Chemical Stimulation. J. Exp. Biol. 1947, 23, 234. [Google Scholar] [CrossRef]
- Le Cointe, R.; Girault, Y.; Morvan, T.; Thibord, J.-B.; Larroudé, P.; Lecuyer, G.; Plantegenest, M.; Bouillé, D.; Poggi, S. Feeding Pests as an {IPM} Strategy: Wireworms in Conservation Agriculture as Case Study. In Proceedings of the 3rd Annual International Branch Virtual Symposium of the Entomological Society of America, 27–29 April 2020. [Google Scholar]
- Hokkanen, H.M.T. Trap Cropping in Pest Management. Ann. Rev. Entomol. 1991, 36, 119–138. [Google Scholar] [CrossRef]
- Miles, H.W.; Petherbridge, F.R. Investigations on the Control of Wireworms. Ann. Appl. Biol. 1927, 14, 359–387. [Google Scholar] [CrossRef]
- Vernon, R.S.; Kabaluk, T.; Behringer, A. Movement of Agriotes Obscurus (Coleoptera: Elateridae) in Strawberry (Rosaceae) Plantings with Wheat (Gramineae) as a Trap Crop. Can. Entomol. 2000, 132, 231–241. [Google Scholar] [CrossRef]
- Landl, M.; Glauninger, J. Preliminary Investigations into the Use of Trap Crops to Control Agriotes Spp. (Coleoptera: Elateridae) in Potato Crops. J. Pest. Sci. 2013, 86, 85–90. [Google Scholar] [CrossRef]
- Adhikari, A.; Reddy, G.V.P. Evaluation of Trap Crops for the Management of Wireworms in Spring Wheat in Montana. Arthropod Plant. Interact. 2017, 11, 755–766. [Google Scholar] [CrossRef]
- Sharma, A.; Sandhi, R.K.; Briar, S.S.; Miller, J.H.; Reddy, G.V.P. Assessing the Performance of Pea and Lentil at Different Seeding Densities as Trap Crops for the Management of Wireworms in Spring Wheat. J. Appl. Entomol. 2019, 143, 460–469. [Google Scholar] [CrossRef]
- Staudacher, K.; Schallhart, N.; Thalinger, B.; Wallinger, C.; Juen, A.; Traugott, M. Plant Diversity Affects Behavior of Generalist Root Herbivores, Reduces Crop Damage, and Enhances Crop Yield. Ecol. Appl. 2013, 23, 1135–1145. [Google Scholar] [CrossRef] [PubMed]
- Thibord, J.-B.; Larroudé, P.; Tour, M.; Ogier, J.C.; Barsics, F. Le Dossier Taupins: Nouvelles Stratégies—Les Solutions à Venir s’inspirent de La Nature. Perspect. Agric. 2015, 427, 58–62. [Google Scholar]
- Furlan, L.; Benvegnù, I.; Chiarini, F.; Loddo, D.; Morari, F. Meadow-Ploughing Timing as an Integrated Pest Management Tactic to Prevent Soil-Pest Damage to Maize. Eur. J. Agron. 2020, 112, 125950. [Google Scholar] [CrossRef]
- Furlan, L.; Pozzebon, A.; Duso, C.; Simon-Delso, N.; Sánchez-Bayo, F.; Marchand, P.A.; Codato, F.; Bijleveld van Lexmond, M.; Bonmatin, J.-M. An Update of the Worldwide Integrated Assessment (WIA) on Systemic Insecticides. Part 3: Alternatives to Systemic Insecticides. Environ. Sci. Pollut. Res. 2018. [Google Scholar] [CrossRef] [Green Version]
Elateridae Species | Crop | Tool | Threshold (Larvae/Trap) | Threshold (Beetles/Season) | Threshold | Reference |
---|---|---|---|---|---|---|
Agriotes brevis | Maize | Bait trap | 1 | [35,57] | ||
Agriotes sordidus | Maize | Bait trap | 2 | [35,57] | ||
Agriotes ustulatus | Maize | Bait trap | 5 | [35,57] | ||
Agriotes lineatus | Maize | Bait trap | 1–2 (seeding before 1st May) | [80] * | ||
Agriotes brevis | Maize | Yf pheromone trap | 210/450 | [57] | ||
Agriotes sordidus | Maize | Yf pheromone trap | 1100 | [57] | ||
Agriotes ustulatus | Maize | Yf pheromone trap | 1000 | [57] | ||
Melanotus communis | Sugarcane | Soil samples taken in sequence to 25 | 8 wireworms found in total samples | [82] |
Alternative Strategies | IPM Principles ** | Section Reference | Damage Reduction Potential | Applicability | Current Implementation |
---|---|---|---|---|---|
Continuous monitoring* integrated with risk assessment | P2: Monitoring (observation, forecast, diagnostics) | 2.1/2.2 | High | Already applied | |
Continuous monitoring * integrated with risk assessment | P3: Decision based on monitoring and thresholds | 2.2.3 | Medium | Already applied | |
Low risk rotation | P1: Prevention and suppression 1.2 Rotation | 3.1.1 | High | High | Already applied |
Tillage | P1: Prevention and suppression 1.2 Rotation | 3.1 | High | High | Already applied |
Biocidal cover crops | P1: Prevention and suppression 1.2 Rotation | 3.1 | Medium | Medium | Already applied |
Identifying optimal planting/sowing and harvest conditions | P1: Prevention and suppression 1.3 Crop management and ecology | 3.1.2 | Medium/high (potato), low/medium others | High | Already applied |
Biocidal materials | P4: Intervention 4.1 Non-chemical methods | 3.4 | Medium | Medium | Already applied |
Larvae biocontrol using attract-and-kill device | P4: Intervention 4.1 Non-chemical methods | 3.3.7 / 3.3.8 | Medium/high | Medium | Under development |
Tolerant varieties | P1: Prevention and suppression 1.3 Crop management and ecology | 3.1 | Medium/high (potato), low/medium others | Medium | Under study |
Adult biocontrol using attract-and-kill device | P4: Intervention 4.1 Non-chemical methods | 3.3.7 / 3.3.9 | Medium | Medium | Under study |
Larvae biocontrol using EPN | P4: Intervention 4.1 Non-chemical methods | 3.3.7 / 3.3.10 | Low/Medium | Medium | Under study |
Habitat - landscape modifications | P1: Prevention and suppression 1.1 Combinations of tactics and multi-pest approach | 3.4 | Medium | Low/medium | Under study |
Protecting the sensitive crop with attractive companion plants | P1: Prevention and suppression 1.3 Crop management and ecology | 4.2 | Medium | ? | Under study |
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Poggi, S.; Le Cointe, R.; Lehmhus, J.; Plantegenest, M.; Furlan, L. Alternative Strategies for Controlling Wireworms in Field Crops: A Review. Agriculture 2021, 11, 436. https://doi.org/10.3390/agriculture11050436
Poggi S, Le Cointe R, Lehmhus J, Plantegenest M, Furlan L. Alternative Strategies for Controlling Wireworms in Field Crops: A Review. Agriculture. 2021; 11(5):436. https://doi.org/10.3390/agriculture11050436
Chicago/Turabian StylePoggi, Sylvain, Ronan Le Cointe, Jörn Lehmhus, Manuel Plantegenest, and Lorenzo Furlan. 2021. "Alternative Strategies for Controlling Wireworms in Field Crops: A Review" Agriculture 11, no. 5: 436. https://doi.org/10.3390/agriculture11050436