The lure of hidden death: development of an attract-and-kill strategy against Agriotes obscurus (Coleoptera: Elateridae) combining semiochemicals and entomopathogenic nematodes

The lure of hidden death: development of an attract-and-kill strategy against Agriotes obscurus (Coleoptera: Elateridae) combining semiochemicals and entomopathogenic nematodes

Abstract: Wireworms are polyphagous soil-dwelling pests that are hard to control. Attract-and-kill strategies, combining attractive semiochemicals with biocontrol agents, have great promise to control insect pests. We hypothesized that the combination of plant semiochemicals and entomopathogenic nematodes (EPNs) in an attract-and-kill system could greatly enhance the nematodes’ efficiency against wireworms. We evaluated the potential of alginate beads loaded with plant extracts and EPNs to control Agriotes obscurus. We tested the efficiency to kill wireworms or to reduce their feeding activity when combining potato tuber extracts as attractants with any of seven different EPN populations. While a direct application of EPNs on wireworms did not reduce the feeding activity nor increased their mortality, the combination of attractants and EPNs encapsulated in alginate beads resulted in attraction and consumption of the EPNs and caused up to 50% wireworm mortality with the EPN species Steinernema carpocapsae. Beads with EPNs caused a significant reduction of the wireworms’ feeding activity. This study shows that wireworms feeding on EPN-containing beads have their feeding activity and survival negatively affected. Considering their long developmental time and the survival capability of EPNs in the soil, implementing this attract-and-kill system in the field might be a suitable strategy for the long-term management of wireworms.Key words: Attract-and-kill, Coleoptera, entomopathogenic nematodes, encapsulation, feeding attractants

___

  • Ansari MA, Evans M, Butt TM (2009). Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Protection 28 (3): 269-272.
  • Barsics F, Delory BM, Delaplace P, Francis F, Fauconnier ML et al. (2017). Foraging wireworms are attracted to root-produced volatile aldehydes. Journal of Pest Science 90 (1): 69-76.
  • Birch N, Glare T (2020). Biopesticides for sustainable agriculture. Cambridge, UK: Burleigh Dodds Science Publishing Limited.
  • Blanco-Pérez R, Bueno-Pallero FÁ, Neto L, Campos-Herrera R (2017). Reproductive efficiency of entomopathogenic nematodes as scavengers. Are they able to fight for insect’s cadavers? Journal of Invertebrate Pathology 148: 1-9.
  • Blanco-Pérez R, Bueno-Pallero FÁ, Vicente-Díez I, Marco-Mancebón VS, Pérez-Moreno I et al. (2019). Scavenging behavior and interspecific competition decrease offspring fitness of the entomopathogenic nematode Steinernema feltiae. Journal of Invertebrate Pathology 164: 5-15.
  • Burnell AM, Stock SP (2000). Heterorhabditis, Steinernema and their bacterial symbionts—Lethal pathogens of insects. Nematology (2): 31-42.
  • Campbell L, Gaugler R (1991). Mechanisms for exsheathment of entomopathogenic nematodes. International Journal of Parasitology (21): 219-224.
  • Campos-Herrera R, Gutiérrez C (2009). Screening Spanish isolates of steinernematid nematodes for use as biological control agents through laboratory and greenhouse microcosm studies. Journal of Invertebrate Pathology 100 (2): 100-105.
  • Campos-Herrera R (Ed.) (2015). Nematode Pathogenesis of Insects and Other Pests. Cham, Switzerland: Springer International Publishing.
  • Eidt DC, Thurston GS (1995). Physical deterrents to infection by entomopathogenic nematodes in wireworms (Coleoptera: Elateridae) and other soil insects. Canadian Entomology 127 (3): 423-429.
  • Ester A, Huiting H (2007). Controlling wireworms (Agriotes spp.) in a potato crop with biologicals. Bulletin OILB/SROP 30: 189-196.
  • Forschler BT, Gardner WA (1991). Parasitism of Phyllophaga hirticula (Coleoptera: Scarabaeidae) by Heterorhabditis heliothidis and Steinernema carpocapsae. Journal of Invertebrate Pathology 58 (3): 396-407.
  • Furlan L (1989). Analisi delle possibilità di riduzione dell’impiego di geodisinfestanti nella coltura del mais nel Veneto. L’Informatore Agrario. 17: 107-115.
  • Furlan L (2004). The biology of Agriotes sordidus Illiger (Col., Elateridae). Journal of Applied Entomology 128 (9-10): 696- 706.
  • Gfeller A, Laloux M, Barsics F, Kati DE, Haubruge E, Du Jardin P, Verheggen F, Lognay, G, Wathelet JP, Fauconnier ML (2013). Characterization of volatile organic compounds emitted by barley (Hordeum vulgare L.) roots and their attractiveness to wireworms. Journal of Chemical Ecology 39 (8): 1129-1139.
  • Grewal PS (2000a) Anhydrobiotic potential and long-term storage of entomopathogenic nematodes (Rhabditida: Steinernematidae). International Journal of Parasitology 30: 995-1000. doi: 10.1016/s0020 -7519(00)00080-1
  • Griffin CT (2015). Behaviour and population dynamics of entomopathogenic nematodes following application. In: Nematode Pathogenesis of Insects and Other Pests. Cham, Switzerland: Springer International Publishing, pp. 57-95.
  • Hazir S, Kaya HK, Stock SP, Keskin N (2003). Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turkish Journal of Biology 27: 181-202.
  • Hiltpold I, Hibbard BE, French BW, Turlings TCJ (2012). Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm. Plant Soil 358: 11-25.
  • Hiltpold I (2015). Prospects in the application technology and formulation of entomopathogenic nematodes for biological control of insect pests. In: Nematode pathogenesis of insects and other pests (pp. 187-205). Cham, Switzerland: Springer International Publishing.
  • Hiltpold I, Jaffuel G, Turlings TC (2015). The dual effects of rootcap exudates on nematodes: from quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes. Journal of Experimental Botany 66 (2): 603-611.
  • Jactel H, Verheggen F, Thiéry D, Escobar-Gutiérrez AJ, Gachet E et al. (2019). Alternatives to neonicotinoids. Environment International 129:423-429.
  • Jaffuel G, Sbaiti I, Turlings TC (2020). Encapsulated Entomopathogenic Nematodes Can Protect Maize Plants from Diabrotica balteata Larvae. Insects, 11 (1): 27.
  • Jansson RK, Seal DR (1994). Biology and management of wireworms on potato. Advances in Potato Pest Biology and Management. St. Paul, MN, USA: APS Press, pp. 31-53.
  • Johnson SN, Gregory PJ (2006). Chemically-mediated host-plant location and selection by root-feeding insects. Physiological Entomology 31 (1): 1-13.
  • Kapranas A, Sbaiti I, Degen T, Turlings TC (2020). Biological control of cabbage fly Delia radicum with entomopathogenic nematodes: selecting the most effective nematode species and testing a novel application method. Biological Control. 104212.
  • Kaya HK, Aguillera MM, Alumai A, Choo HY, De la Torre M et al. (2006). Status of entomopathogenic nematodes and their symbiotic bacteria from selected countries or regions of the world. Biological Control 38 (1): 134-155.
  • Kaya HK, Nelsen CE (1985). Encapsulation of steinernematid and heterorhabditid nematodes with calcium alginate: a new approach for insect control and other applications. Environmental Entomology 14 (5): 572-574.
  • Kim J, Jaffuel G, Turlings TCJ (2014). Enhanced alginate capsule properties as a formulation of entomopathogenic nematodes. BioControl 60: 527-535.
  • Kim J, Hiltpold I, Jaffuel G, Sbaiti I, Hibbard BE et al. (2021). Calcium-alginate beads as a formulation for the application of entomopathogenic nematodes to control rootworms. Journal of Pest Science 1-12.
  • Koppenhöfer AM (2007). Nematodes. In Field Manual of Techniques in Invertebrate Pathology; Lacey, L.A., Kaya, H.K., Eds.; Springer: Dordrecht, The Netherlands,; pp. 249-264.
  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M et al. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology 132: 1-41.
  • la Forgia D, Verheggen F (2017). The law of attraction: identification of Volatiles Organic Compound emitted by potatoes as wireworm attractants. Communication in Agricultural and Applied Biological Science 82 (2): 167-169.
  • la Forgia D, Verheggen F (2019). Biological alternatives to pesticides to control wireworms (Coleoptera: Elateridae). Agrigene, 100080.
  • la Forgia D, Jaffuel G, Campos-Herrera R, Verheggen F, Turlings TC (2020). Efficiency of an attract-and-kill system with entomopathogenic nematodes against wireworms (Coleoptera: Elateridae). IOBC-WPRS Bulletin, 150: 91-95.
  • Lewis EE, Hazir S, Hodson A, Gulcu B (2015). Trophic relationships of en- tomopathogenic nematodes in agricultural habitats. In: Campos-Herrera, R. (Ed.), Nematode pathogeneses of insects and other pests. Springer International Publishing, Switzerland, pp. 139-163.
  • Morton A, Garcia-del-Pino F (2016). Laboratory and field evaluation of entomopathogenic nematodes for control of Agriotes obscurus (L.)(Coleoptera: Elateridae). Journal of Applied Entomology 141 (4): 241-246.
  • Mráček Z, Růžička Z (1990). Infectivity and development of Steinernema sp. strain Hylobius (Nematoda, Steinernematidae) in aphids and aphidophagous coccinellids. Journal of Applied Entomology 110 (1-5): 92-95.
  • Parker WE, Howard JJ (2001). The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agricultural and Forest Entomology 3 (2): 85-98.
  • Rahatkhah Z, Karimi J, Ghadamyari M, Brivio MF (2015). Immune defenses of Agriotes lineatus larvae against entomopathogenic nematodes. BioControl 60: 641-653.
  • Sandhi RK, Shapiro-Ilan D, Sharma A, Reddy GV (2020). Efficacy of entomopathogenic nematodes against the sugarbeet wireworm, Limonius californicus (Mannerheim)(Coleoptera: Elateridae). Biological Control 104190.
  • Shapiro-Ilan, DI, Gouge D, Koppenhöfer AM (2002). Factors affecting eld ef cacy: analysis of case studies in cotton, turf, and citrus. In: Gaugler, R. (Ed.), Entomopathogenic Nematology. CABI Publishing, Wallingford, UK, pp. 333-356.
  • Shapiro-Ilan DI, Han R, Dolinksi C (2012). Entomopathogenic nematode production and application technology. Journal of Nematology 44 (2): 206.
  • Toba HH, Lindegren JE, Turner JE, Vail PV (1983). Susceptibility of the Colorado potato beetle and the sugarbeet wireworm to steinernema feltiae and s. Glaseri. Journal of Nematology 15: 597-601.
  • Traugott M, Benefer CM, Blackshaw RP, van Herk WG, Vernon RS (2015). Biology, ecology, and control of elaterid beetles in agricultural land. Annual Review of Entomology 60: 313-334.
  • Zhao KJ, Zhang LK, Song J, Zhang LH, Li GX et al. (1996). On the application of steinernematid nematodes against eight lepidopterous and coleopterous insect pests. Acta Phytophylacica Sin. 23 (1): 20-24.
  • White GF (1927). A method for obtaining infective nematode larvae from cultures. Science (Washington), 66 (1709).
Turkish Journal of Zoology-Cover
  • ISSN: 1300-0179
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

Compatibility of entomopathogenic nematodes with plant extracts and post-exposure virulence test under laboratory condition

Adeola Abiola OSO, Tshimangadzo RAMAKUWELA, Anofi Omotayo Tom ASHAFA

Assessment of the zooplankton community structure of the coastal Uzungol Lagoon (Kizilirmak Delta, Turkey) based on community indices and physicochemical parameters

Ceren Deniz ÖZDEMİR, Yasemin SAYGI, Ertunç GÜNDÜZ, Fatma Yıldız DEMİRKALP, Çağaşan KARACAOĞLU

Sedat PER, Kubra CUBUKCU, Ayse TOLUK, Nusret AYYİLDİZ

Abbas GUNGORDU, Nesrin OZMEN, Sema ERDEMOGLU, Duygu Ozhan TURHAN, Meltem ASİLTURK, Emrah AKGEYİK, Murat OZMEN

Yigit Ali TATLİ, Refik BOZBUGA, Goksel OZER, Fouad MOKRİNİ, Rachid LAHLALİ, Abdelfattah DABABAT, Mustafa IMREN

Identification and characterisation of crustacean hyperglycaemic hormone (CHH) from Mediterranean shore crab Carcinus aestuarii

Marsilda QYLİ, Valbona ALİKO, Riccardo SGARRA, Piero Giulio GİULİANİNİ, Chiara MANFRİN

Evaluation on reducing toxicity of fluoxastrobin with doped TiO2 nanoparticles

Emrah AKGEYİK, Duygu ÖZHAN TURHAN, Abbas GÜNGÖRDÜ, Nesrin ÖZMEN, Meltem ASİLTURK, Murat ÖZMEN, Sema ERDEMOĞLU

Marsilda QYLİ, Valbona ALİKO, Riccardo SGARRA, Piero Giulio GİULİANİNİ, Chiara MANFRİN

Yun-chun YE, Yi LUO, Zhao-min ZHOU

Determining some biological parameters of Aenasius arizonensis (Girault) (Hymenoptera: Encyrtidae) on cotton mealybug and the rate of parasitism in field conditions

Asime Filiz ÇALIŞKAN KEÇE, Mehmet Rifat ULUSOY, Doğancan KAHYA