The use of entomopathogenic nematodes in the control of stored-product insects

Christos I. Rumbos1, Christos G. Athanassiou1
1Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Phytokou str., N. Ionia, Magnesia, 38446, Volos, Greece

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Adarkwah C, Ulrichs C, Schaarschmidt S, Badii BK, Addai IK, Obeng-Ofori D, Schöller M (2014) Potential of Hymenopteran larval and egg parasitoids to control stored-product beetle and moth infestation in jute bags. B Entomol Res 104:534–542

Alikhan MA, Bednarek A, Grabiec S (1985) The physiological and morphological characteristics of Neoaplectana carpocapsae (Nematoda, Steinernematidae) in two insect hosts. J Invertebr Pathol 45:168–173

Arthur FH, Subramanyam B (2012) Chemical control in stored products. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection, S156. Kansas State University, Manhattan, pp 95–100

Arthurs S, Heinz KM, Prasifka JR (2004) An analysis of using entomopathogenic nematode against above ground pests. B Entomol Res 94:297–306

Athanassiou CG, Palyvos NE, Kakouli-Duarte T (2008) Insecticidal effect of Steinernema feltiae (Filipjev) (Nematoda: Steinernematidae) against Tribolium confusum du Val (Coleoptera: Tenebrionidae) and Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) in stored wheat. J Stored Prod Res 44:52–57

Athanassiou CG, Kavallieratos NC, Menti H, Karanastasi E (2010) Mortality of four stored product pests in stored wheat when exposed to doses of three entomopathogenic nematodes. J Econ Entomol 103:977–984

Atwa AA, Hegazi EM, Khafagi WE, Abd El-Aziz GM (2013) Interaction of the koinobiont parasitoid Microplitis rufiventris of the cotton leafworm, Spodoptera littoralis, with two entomopathogenicrhabditids, Heterorhabditis bacteriophora and Steinernema carpocapsae. J Insect Science 13:84

Baker K, Cook RJ (1982) Biological control of plant pathogens. The American Phytopathological Society, St. Paul

Barbosa-Negrisoli CRDC, Negrisoli ASJ, Bernardi D, Garcia MS (2013) Activity of eight strains of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) against five stored product pests. Exp Parasitol 134:384–388

Baxter IH (2008) Entomopathogen based autodissemination for the control of Plodia interpunctella (Hübner)—an examination of the critical components. Dissertation, University of Southampton, pp 149

Baxter IH, Howard N, Armsworth CG, Barton LEE, Jackson C (2008) The potential of two electrostatic powders as the basis for an autodissemination control method of Plodia interpunctella (Hübner). J Stored Prod Res 44:152–161

Bedding RA, Molyneux AS, Akhurst RJ (1983) Heterororhabditis spp., Neoaplectana spp. and Steinernema kraussei: interspecific and intraspecific differences in infectivity for insects. Exp Parasitol 55:249–257

Belair G, Fournier Y, Dauphinais N (2003) Efficacy of steinernematid nematodes against three insect pests of crucifers in Quebec. J Nematol 35:259–265

Brower JH, Smith L, Vail PV, Flinn PW (1996) Biological control. In: Subramanyam B, Hagstrum DW (eds) Integrated management of insect in stored products pest. Dekker, New York, pp 223–286

Byers JA, Poinar GO Jr (1982) Location of insect hosts by the nematode, Neoaplectana carpocapsae, in response to temperature. Behaviour 79:1

Cabanillas HE, Poinar GO, Raulston JR (1994) Steinernema riobravis n. sp. (Rhabditida: Steinernematidae) from Texas. Fund Appl Nematol 17:123–131

Campbell JF, Gaugler R (1997) Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum? Fund Appl Nematol 20:393–398

Choo HY, Lee DW, Yoon HS, Lee SM, Hang DT (2002) Effects of temperature and nematode concentration on virulence and reproduction of entomopathogenic nematode, Steinernema carpocapsae Pocheon strain (Nematoda: Steinernematidae). Korean J Appl Entomol 41:269–277

Ciche TA, Darby C, Ehlers RU, Forst S, Goodrich-Blair H (2006) Dangerous liaisons: the symbiosis of entomopathogenic nematodes and bacteria. Biol Control 38:22–46

Collins PJ, Lambkin TM, Bridgeman BW, Pulvirenti C (1993) Resistance to grain protectant insecticides in coleopterous pests of stored cereals in Queensland, Australia. J Econ Entomol 86:239–245

Connick WJ (1988) Formulation of living biological control agents with alginate. In: pesticide formulations, ACS Symposium Series. American Chemical Society, pp 241–250

Doucet MMA, de Miranda MB, Bertolotti MA, Caro KA (1996) Efficacy of Heterorhabditis bacteriophora (strain OLI) in relation to temperature, concentration and origin of the infective juvenile. Nematropica 26:129–133

Dowds BCA, Peters A (2002) Virulence mechanisms. In: Gaugler R (ed) Entomopathogenic nematology. CABI, New York, pp 79–98

Ehlers RU (2003) Entomopathogenic nematodes in the European biocontrol market. Commun Agric Appl Biol Sci 68:3–16

Ehlers RU (2005) Forum on safety and regulation. In: Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 107–114

Fields PG (1992) The control of stored-product insects and mites with extreme temperatures. J Stored Prod Res 28:89–118

Flinn PW, Schöller M (2012) Biological control: Insect pathogens, parasitoids, and predators. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection, S156. Kansas State University, Manhattan, pp 203–212

Gaugler R (1988) Ecological considerations in the biological control of soil-inhabiting insects with entomopathogenic nematodes. Agr Ecosyst Environ 24:351–360

Gaugler R (2002) Entomopathogenic entomology. CABI Publishing, Wallingford

Gaugler R, LeBeck L, Nakagaki B, Boush GM (1980) Orientation of the entomopathogenous nematode, Neoaplectana carpocapsae, to carbon dioxide. Environ Entomol 8:658

Gaugler R, Grewal PS, Kaya HK, Smith-Fiola D (2000) Quality assessment of commercially produced entomopathogenic nematodes. Biol Control 17:100–109

Geden CJ, Axtell RC, Brooks WM (1985) Susceptibility of the lesser mealworm Alphitobius diaperinus (Coleoptera: Tenebrionidae) to the entomogenous nematodes Steinernema feltiae, S. glaseri (Steinernematidae) and Heterorhabditis heliothidis (Heterorhabditidae). J Entomol Sci 20:331–339

Grewal PS (2002) Formulation and application technology. In: Gaugler R (ed) Entomopathogenic Nematology, CABI Publishing. Wallingford, UK, pp 265–287

Grewal PS (2012) Entomopathogenic nematodes as tools in integrated pest management. In: Abrol DP (ed) Integrated pest management: principles and practice. CABI Publishing, Wallingford, pp 162–236

Grewal PS, Selvan S, Gaugler R (1994) Thermal adaptation of entomopathogenic nematodes—niche breadth for infection, establishment and reproduction. J Thermal Biol 19:245–253

Guedes RNC, Dover BA, Kambhampati S (1996) Resistance to chlorpyrifosmethyl, pirimiphos-methyl, and malathion in Brazilian and US populations of Rhyzopertha dominica (Coleoptera: Bostrichidae). J Econ Entomol 89:27–32

Hasselmann K, Stevens AD, Heffele D (2005) Investigations towards a biological control of cockroaches with entomopathogenic nematodes. Gesunde Pflanzen 57:169–178

Hazir S, Stock SP, Kaya HK, Koppenhöfer AM, Keskin N (2001) Developmental temperature effects on five geographic isolates of the entomopathogenic nematode Steinernema feltiae (Nematoda: Steinernematidae). J Invertebr Pathol 77:243–250

Hiltpold I, Hibbard BE, Wade FB, Turlings TCJ (2012) Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the Western corn rootworm. Plant Soil 358:11–25

Hsiao WF, All JN (1996) Effects of temperature and placement site on the dispersal of the entomopathogenic nematode, Steinernema carpocapsae in four soils. Chin J Entomol 16:95–106

Hubert J, Nesvorna M, Volek V (2015) Stored product mites (Acari: Astigmata) infesting food in various types of packaging. Exp Appl Acarol 65:237–242

Ishibashi N, Kondo E (1990) Behavior of infective juveniles. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 139–152

Kavallieratos NG, Athanassiou CG, Aountala M, Kontodimas DC (2014) Evaluation of the entomopathogenic fungi Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea for control of Sitophilus oryzae. J Food Protect 77:87–93

Kaya HK (1990) Soil ecology. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 93–115

Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Ann Rev Entomol 38:181–206

Kaya HK, Nelsen CE (1985) Encapsulation of steinernematid and heterorhabditid nematodes with calcium alginate: a new approach for insect control and other applications. Environ Entomol 14:572–574

Kim J, Jaffuel G, Turlings TCJ (2015) Enhanced alginate capsule properties as a formulation of entomopathogenic nematodes. Biocontrol 60:527–535

Koehler PG, Patterson RS, Martin WR (1992) Susceptibility of cockroaches (Dictyoptera: Blattellidae, Blattidae) to infection by Steinernema carpocapsae. J Econ Entomol 85:1184–1187

Koppenhöfer AM, Grewal PS (2005) Compatibility with agrochemicals and other biocontrol agents. In: Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, pp 363–382

Koppenhöfer AM, Kaya HK, Taormino SP (1995) Infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae) at different soil depths and moistures. J Invertebr Pathol 65:193–199

Koppenhöfer AM, Choo HY, Kaya HK, Lee DW, Gelernter WD (1999) Increased field and greenhouse efficacy against scarab grubs with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biol Control 14:37–44

Koppenhöfer AM, Brown IM, Gaugler R, Grewal PS, Kaya HK, Klein MG (2000) Synergism of entomopathogenic nematodes and imidacloprid against white grubs: greenhouse and field evaluation. Biol Control 19:245–251

Kung SP, Gaugler R, Kaya HK (1991) Effects of soil temperature, moisture, and relative humidity on entomopathogenic nematode persistence. J Invertebr Pathol 57:242–249

Lacey LA, Unruh TR, Headrick HL (2003) Interactions of two idiobiont parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). J Invertebr Pathol 83:230–239

Lanzoni A, Ade G, Martelli R, Radeghieri P, Pezzi F (2014) Technological aspects of Steinernema carpocapsae spray application alone or mixed with Bacillus thuringiensis aizawai in spinach crop. B Insectol 67:115–124

Laznik Z, Tóth T, Lakatos T, Vidrih M, Trdan S (2010) The activity of three new strains of Steinernema feltiae against adults of Sitophilus oryzae under laboratory conditions. J Food Agric Environ 8:150–154

Lord JC, Campbell JF, Sedlacek JD, Vail PV (2007) Application and evaluation of entomopathogens for managing insects in stored products. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology, 2nd edn. Springer, Dordrecht, pp 677–693

Mason LJ, McDonough M (2012) Biology, behavior, and ecology of stored grain and legume insects. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored product protection, S156. Kansas State University, Manhattan, pp 7–20

Mbata GN, Shapiro-Ilan DI (2005) Laboratory evaluation of virulence of Heterorhabditid nematodes to Plodia interpunctella Hübner (Lepidoptera:Pyralidae). Environ Entomol 34:676–682

Mbata GN, Shapiro-Ilan DI (2010) Compatibility of Heterorhabditis indica (Rhabditida: Heterorhabditidae) and Habrobracon hebetor (Hymenoptera: Braconidae) for biological control of Plodia interpunctella (Lepidoptera: Pyralidae). Biol Control 54:75–82

Menti H, Wright DJ, Perry RN (2000) Infectivity of populations of the entomopathogenic nematodes Steinernema feltiae and Heterorhabditis megidis in relation to temperature, age and lipid content. Nematology 2:515–521

Moore D, Lord JC, Smith SM (2000) Pathogens. In: Subramanyam B, Hagstrum DW (eds) Alternatives to pesticides in stored product IPM. Kluwer Academic Publishers, Dordrecht, pp 193–227

Morris ON (1985) Susceptibility of 31 species of agricultural pests to entomogenous nematodes Steinernema feltiae and Heterorhabditis bacteriophora. Can Entomol 122:309–320

Morton A, García-del-Pino F (2013) Sex-related differences in the susceptibility of Periplaneta americana and Capnodis tenebrionis to the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 112:203–207

Navaneethan T, Strauch O, Besse S, Bonhomme A, Ehlers RU (2010) Influence of humidity and a surfactant-polymer-formulation on the control potential of the entomopathogenic nematode Steinernema feltiae against diapausing codling moth larvae (Cydia pomonella L.) (Lepidoptera: Tortricidae). Biocontrol 55:777–788

Nayak MK, Holloway JC, Emery RN, Pavic H, Bartleta J, Collins PJ (2013) Strong resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae): its characterisation, a rapid assay for diagnosis and its distribution in Australia. Pest Manag Sci 69:48–53

Nguyen KB (2015a) Species of Steinernema. University of Florida, Entomology and Nematology Department.  http://entnem.ifas.ufl.edu/nguyen/morph-/steinsp1.htm . Accessed 10 June 2016

Nguyen KB (2015b) Species of Heterorhabditis. University of Florida, Entomology and Nematology Department. http://entnem.ifas.ufl.edu/nguyen/morph-/HETEROSP.htm . Accessed 10 June 2016

Niedermayer S, Steidle JLM (2013) The Hohenheimer Box—a new way to rear and release Lariophagus distinguendus to control stored product pest insects. Biol Control 64:263–269

Nishimatsu T, Jackson JJ (1998) Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 91:410–418

Opit GP, Phillips TW, Aikins MJ, Hasan MM (2012) Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from stored wheat in Oklahoma. J Econ Entomol 105:1107–1114

Oppert B, Morgan TD, Kramer KJ (2011) Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors against coleopteran storage pests. Pest Manag Sci 67:568–573

Patel AV, Vorlop KD (1994) Entrapment of biological control agents applied to entomopathogenic nematodes. Biotechnol Tech 8:569–574

Pimentel MAG, Faroni LRD, da Silva FH, Batista MD, Guedes RNC (2010) Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotrop Entomol 39:101–107

Poinar GO (1990) Biology and taxonomy of Steinernematidae and Heterorhabditidae. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 23–62

Ramos-Rodríguez O, Campbell JF, Ramaswamy SB (2006) Pathogenicity of three species of entomopathogenic nematodes to some major stored-product insect pests. J Stored Prod Res 42:241–252

Ramos-Rodríguez O, Campbell JF, Ramaswamy SB (2007a) Efficacy of the entomopathogenic nematode Steinernema riobrave against the stored-product insect pests Tribolium castaneum and Plodia interpunctella. Biol Control 40:15–21

Ramos-Rodríguez O, Campbell JF, Christen JM, Shapiro-Ilan DI, Lewis EE, Ramaswamy SB (2007b) Attraction behaviour of three entomopathogenic nematode species towards infected and uninfected hosts. Parasitology 134:729–738

Rasmann S, Turlings TCJ (2008) First insights into specificity of belowground tritrophic interactions. Oikos 117:362–369

Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

Rumbos CI, Athanassiou CG (2012) Insecticidal effect of six entomopathogenic nematode strains against Lasioderma serricorne (F.) (Coleoptera: Anobiidae) and Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae). J Stored Prod Res 50:21–26

Schmidt J, All JN (1979) Chemical attraction of Neoaplectana carpocapsae (Nematoda: Steinernematidae) to common excretory products of insects. Environ Entomol 8:55

Schöller M, Flinn PW (2000) Parasitoids and predators. In: Subramanyam B, Hagstrum DW (eds) Alternatives to pesticides in stored-product IPM. Kluwer Academic Publishers, Norwell, Massachusetts, pp 229–271

Schöller M, Prozell S, Al-Kirshi A-G, Reichmuth Ch (1997) Towards biological control as a major component of integrated pest management in stored product protection. J Stored Prod Res 33:81–97

Shahina F, Salma J (2009) Laboratory evaluation of seven Pakistani strains of entomopathogenic nematode against a stored product insect pest, Pulse beetle (Callosobruchus chinensis L.). J Nematol 41:255–260

Shahina F, Salma J (2010) Laboratory evaluation of seven Pakistani strains of entomopathogenic nematode against a stored product insect pest, rice weevil (Sitophilus oryzae L.). Pak J Nematol 28:295–305

Shahina F, Salma J (2011a) Pakistani strains of entomopathogenic nematode as a biological control agent against stored grain pest, Tribolium castaneum. Pak J Nematol 29:25–34

Shahina F, Salma J (2011b) Virulence of Pakistani isolates of entomopathogenic nematode against a stored insect species, Lasioderma serricorne. Int J Nematol 21:79–85

Shannag HK, Webb SE, Capinera JL (1994) Entomopathogenic nematode effect on pickleworm (Lepidoptera: Pyralidae) under laboratory and field conditions. J Econ Entomol 87:1205–1212

Shapiro-Ilan DI, Mbata GN, Nguyen KB, Peat SM, Blackburn D, Adams BJ (2009) Characterization of biocontrol traits in the entomopathogenic nematode Heterorhabditis georgiana (Kesha strain), and phylogenetic analysis of the nematode’s symbiotic bacteria. Biol Control 51:377–387

Shapiro-Ilan DI, Han R, Dolinksi C (2012) Entomopathogenic nematode production and application technology. J Nematol 44:206–217

Sheykhnejad H, Ghadamyari M, Koppenhöfer AM, Karimi J (2014) Interactions between entomopathogenic nematodes and imidacloprid for rose sawfly control. Biocontrol Sci Techn 24:1481–1486

Simoes N, Rosa JS (1996) Pathogenity and host specificity of entomopathogenic nematodes. Biocontrol Sci Techn 6:403–411

Smart GC (1995) Entomopathogenic nematodes for the biological control of insects. J Nematol 27:529–534

Steiner WA (1996) Dispersal and host-finding ability of entomopathogenic nematodes at low temperatures. Nematologica 42:243–261

Stock SP, Blair HG (2008) Entomopathogenic nematodes and their bacterial symbionts: the inside out of a mutualistic association. Symbiosis 46:65–75

Subramanyam B, Harein PK, Cutkomp LK (1989) Organophosphate resistance in adults of red flour beetle (Coleoptera: Tenebrionidae) and sawtoothed grain beetle (Coleoptera: Cucujidae) infesting barley stored on farms in Minnesota. J Econ Entomol 82:989–995

Svendsen TS, Steenberg T (2000) The potential use of entomopathogenic nematodes against Typhaea stercorea. Biocontrol 45:97–111

Trdan S, Vidrih M, Vali N (2006) Activity of four entomopathogenic nematode species against young adults of Sitophilus granarius (Coleoptera: Curculionidae) and Oryzaephilus surinamensis (Coleoptera: Silvanidae) under laboratory conditions. J Plant Dis Prot 113:168–173

Tulek A, Erturk S, Kepenekci I, Atay T (2015) Efficacy of native entomopathogenic nematodes against the stored grain insect pest, Rhyzopertha dominica (F) (Coleoptera: Bostrichidae) adults. Egypt J Biol Pest Control 25:251–254

van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4:292–294

Vemmer M, Patel AV (2013) Review of encapsulation methods suitable for microbial biological control agents. Biol Control 67:380–389

White NDG (1995) Insects, mites, and insecticides in stored grain ecosystems. In: Jayas DS, White NDG, Muir WE (eds) Stored-grain ecosystems. Marcel Dekker Inc., New York, pp 123–168

Wójcik WF (1986a) Influence of the size of host on the growth of the Neoplectana carpocapsae Weiser, 1955 nematodes. Ann Warsaw Agri Univ SGGW-AR Anim Sci 20:75–85

Wójcik WF (1986b) Effect of worsening of physiological state of insects on the growth of the nematodes, Neoplectana carpocapsae Weiser, 1955. Ann Warsaw Agri Univ SGGW-AR Anim Sci 20:109–111

Wright PJ, Peters A, Schroer S, Fife JP (2005) Application technology. In: Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, pp 91–106

Wu S, Youngman RR, Kok LT, Laub CA, Pfeiffer DG (2014) Interaction between entomopathogenic nematodes and entomopathogenic fungi applied to third instar southern masked chafer white grubs, Cyclocephala lurida (Coleoptera: Scarabaeidae), under laboratory and greenhouse conditions. Biol Control 76:65–73

Yilmaz S, Ayvaz A, Akbulut M, Azizoglu U, Karabörklü S (2012) A novel Bacillus thuringiensis strain and its pathogenicity against three important pest insects. J Stored Prod Res 51:33–40

Zannou ID, Adebo HO, Zannou E, Hell K (2013) Mites associated with stored grain commodities in Benin, West Africa. Exp Appl Acarol 61:449–470

Zettler JL, Arthur FH (2000) Chemical control of stored product insects with fumigants and residual treatments. Crop Prot 19:577–582

Zettler JL, Cuperus GW (1990) Pesticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae) and Rhyzopertha dominica (Coleoptera: Bostrichidae) in wheat. J Econ Entomol 83:1677–1681