Pathogenicity of Steinernema carpocapsae and Heterorhabditis bacteriophora on tomato leafminer, Tuta absoluta

Document Type : Research Paper

Authors

Department of Plant Pathology, Marvdasht Branch, Islamic Azad University

Abstract

Leafminer moth Tuta absoluta is a serious insect pest of tomato crops which could impose upto 100% yield loss. This study was conducted to study the pathogenicity of third stage juveniles (IJs) of Steinernema carpocapsae (Sc) and Heterorhabditis bacteriophora (Hb) on different instars of pest larvae in Petri dish and in a leaf bioassay. The most virulent nematode was selected for the following tests. The ability of different concentrations of the more efficient species in parasitizing the last instar larvae (L4), pupae in Petri dish (50, 100 and 200 IJs/Petri dish) and pupae in soil (50, 100 and 200 IJs/cm2 soil) was determined. In the greenhouse experiment, the efficacy of the selected species against different larval stages was examined and compared with chemical pesticide, indoxacarb. Hb was selected as the most effective species since its controlling ability was approximately 1.7 times more than Sc. 50 IJs of Hb per Petri dish parasitized 84% of pest’ L4. The highest mortality of pupae in Petri dishes (40%) and soil (28%) was achieved when IJs were respectively applied at a rate of 200 IJs/Petri dish and 200 IJs/cm2 soil. Increase in IJs’ concentrations resulted in higher mortality of pupae. In the greenhouse, the most susceptible stage of thr insect pest to Hb was L4, while the chemical pesticide had less effect on pest's larvae. According to the overall results of the study, it seems that Hb could alleviate the damage and produce acceptable control level of the insect pest.

 

Keywords

Main Subjects

Full Text

Abbott, W.S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265–276.

Abootorabi, E. 2014. Report of native isolate pathogenicity of Steinernema feltiae on tomato leafminer, Tuta absoluta. Biocontrol in Plant Protection, 1: 107–109.

Adams, B.J., Fodor, A., Koppenhöfer, H.S., Stackebrandt, E., Stock, S.P. & Klein, M.G. 2006. Biodiversity and systematics of nematode-bacterium entomopathogens. Biological Control, 37: 32–49.

Arnó, J. & Gabarra, R. 2011. Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). Journal of Pest Science, 84: 513–520.

Arthurs, S., Heinz, K.M. & Prasifka, J.R. 2004. An analysis of using entomopathogenic nematodes against above ground pest. Bulletin of Entomological Research, 94: 297–306.

Batalla-Carrera, L., Morton, A. & García-del-Pino, F. 2010. Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl, 55: 523–530.

Begley, J.W. 1990. Efficacy against insects in habitats others than soil. pp. 215–231. In: Gaugler, R. & Kaya, H.K. (eds.), Entomopathogenic Nematodes in Biological Control. CRC Press, Boca Raton.

Campbell, J.F. & Gaugler, R. 1993. Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Behaviour, 126: 155–169.

Desneux, N., Ramirez-Romero, R. & Kaiser, L. 2006. Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environmental Toxicology and Chemistry, 25: 2675–2682.

Desneux, N., Decourtye, A. & Delpuech, J.M. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81–106.

Desneux, N., Wajnberg, E., Wyckhuys., K.A.G., Burgio., G., Arpaia, S., Narvaez-Vasquez, C.A., Gonzalez-Cabrera, J., Ruescas, D.C., Tabone, E., Frandon, J., Pizzol, J., Poncet, C., Cabello, T. & Urbaneja, A. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science, 83: 197–215.

Desneux, N., Luna, M.G., Guillemaud, T. & Urbaneja, A. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. Journal of Pest Science, 84: 403–408.

Divya, K., Sankar, M. 2009. Entomopathogenic nematodes in pest management. Indian Journal of Science and Technology, 2: 53–60.

Do Thi Khanh, H., Chailleux, A., Tiradon, M., Desneux, N., Colombel, E. & Tabone, E. 2012. Using new egg parasitoids (Trichogramma spp.) to improve integrated management against Tuta absoluta. Bulletin OEPP/EPPO Bulletin, 42: 249–254.

Dowds, B.C.A. & Peters, A. 2002. Virulence mechanisms. pp. 79–98. In: Gaugle, R. (ed.), Entomopathogenic Nematology. CAB International, Wallingford.

Ebssa, L. & Koppenhöfer, A.M. 2012. Entomopathogenic nematodes for the management of Agrotis ipsilon: effect of instar, nematode species and nematode production method. Pest Management Science, 68: 947–957.

Ehlers, R.U., Shapiro-Ilan, D.I. 2005. Mass production. pp. 65–78. In: Grewal, P.S., Ehlers, R.U. & Shapiro-Ilan, D.I. (eds.), Nematodes as Biocontrol Agents. CAB International, Wallingford.

Gabarra, R., Arnó, J., Lara, L., Verdú, M.J., Ribes, A., Beitia, F., Urbaneja, A., Téllez, M. Del M., Mollá & O., Riudavets, J. 2014. Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast. Biocontrol, 59: 45–54.

Garcia-del-Pino, F., Alabern, X. & Morton, A. 2013. Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl, 58: 723–731.

Ghoneim, K. 2014. Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. Journal of Entomology and Zoology Studies, 2: 52–71.

Griffin, C.T., Boemare, N.E. & Lewis, E.E. 2005. Biology and behavior. pp. 47–64. In: Grewal, P.S., Ehlers, R.U. & Shapiro-Ilan, D.I. (eds.), Nematodes as Biocontrol Agents. CAB International, Wallingford.

Hallem, E.A., Dillman, A.R., Hong, A.V., Zhang, Y., Yano, J.M., DeMarco, S.F. & Sternberg, P.W. 2011. A sensory code for host seeking in parasitic nematodes. Current Biology, 21: 377–383.

Hominick, W.M. 2002. Biogeography. pp. 115–143. In: Gaugler, R. (ed.), Entomopathogenic Nematology. CABI Publishing, Wallingford.

Hunt, D.J. 2007. Introduction. pp. 1–26. In: Nguyen, K.B. & Hunt, D.J. (eds.), Hunt, D.J. & Perry, R.N. (Series eds.), Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts, Nematology Monographs and Perspectives. Koninklijke Brill NV, Leiden.

Jackson, J.J., Brooks, M.A. 1995. Parasitism of western corn rootworm larvae and pupae by Steinernema carpocapsae. Nematology, 27: 15–20.

Kaya, H.K. & Stock, S.P. 1997. Techniques in insect nematology. pp. 281–324. In: Lacey, L. (ed.), Manual of Techniques in Insect Pathology. Academic Press, San Diego.

Kim, H.H., Choo, H.Y., Kaya, H.K., Lee, D.W., Lee, S.M. & Jeon, H.Y. 2004. Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biological control agent against the fungus gnat Bradysia agrestis (Diptera: Sciaridae) in propagation houses. Biocontrol Science and Technology, 14: 171–183.

Koppenhöfer, A.M. 2000. Nematodes. pp. 283–301. In: Lacey, L.A. & Kaya, H.K. (eds.), Field Manual of Techniques in Invertebrate Pathology. Kluwer, Dordrecht.

Koppenhöfer, A.M. & Kaya, H.K. 2002. Entomopathogenic nematodes and insect pest management. pp. 258–313. In: Koul, O. & Dhaliwal, G.S. (eds.) Microbial Biopesticides. Taylor & Francis, Abingdon.

Lacey, L.A. & Georgis, R. 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44: 218–225.

Lewis, E.E. 2002. Behavioural ecology. pp. 205–223. In: Gaugle, R. (ed.), Entomopathogenic Nematology, CAB International, Wallingford.

Lewis, E.E., Gaugler, R. & Harrison, R. 1993. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Canadian Journal of Zoology, 71: 765–769.

Lewis, E.E., Grewal, P.S. & Gaugler, R. 1995. Hierarchical order of host cues in parasite foraging strategies. Parasitology, 110: 207–213.

Lietti, M.M.M., Botto, E. & Alzogaray, P.A. 2005. Insecticide Resistance in Argentine Populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology, 34: 113–119.

Metwally, H.M.S., Hafez, G.A., Hussein, M.A., Hussein, M.A., Salem, H.A. & Saleh, M.M.E. 2012. Low cost artificial diet for rearing the greater wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae) as a host for entomopathogenic nematodes. Egyptian Journal of Biological Pest Control, 22: 15–17.

Moosavi, M.R. & Zare, R. 2012. Fungi as biological control agents of plant-parasitic nematodes. pp: 67–107. In: Merillon, J.M. & Ramawat, K.G. (eds.), Plant Defence: Biological Control, Progress in Biological Control 12. Springer Science + Business Media, Dordrecht.

Moosavi, M.R. & Askary, T.H. 2015. Nematophagous fungi- Commercialization. pp: 187–202. In: Askary, T.H. & Martinelli, P.R.P. (eds.), Biocontrol Agents of Phytonematodes. CABI Publishing, Wallingford.

Nannini, M., Atzori, F., Murgia, G., Pisci, R. & Sanna, F. 2012. Use of predatory mirids for control of the tomato borer Tuta absoluta (Meyrick) in Sardinian greenhouse tomatoes. Bulletin OEPP/EPPO Bulletin, 42: 255–259.

Nguyen, K.B. 2007. Methodology, morphology and identification. pp. 59–119. In: Nguyen, K.B. & Hunt, D.J. (eds.) Hunt, D.J. & Perry, R.N. (series eds.), Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts, Nematology Monographs and Perspectives. Koninklijke Brill NV, Leiden.

Poinar, G.O. Jr. 1976. Description and biology of a new insect parasitic rhabditoid, Heterorhabditis bacteriophora n. gen., n. sp. (Rhabditida: Heterorhabditidae n. fam.). Nematologica, 21:463–470.

Půža, V. 2015. Control of insect pests by entomopathogenic nematodes. pp. 175–183. In: Lugtenberg, B. (ed.), Principles of Plant-Microbe Interaction. Springer International Publishing, Bern.

Riquelme, V.M., Botto, E.N. & Lafalce, C. 2006. Efficacy of insecticides against the “Tomato moth”, Tuta absoluta (Lepidoptera: Gelechiidae) and their residual effects on the parasitoid Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae). Revista de la Sociedad Entomológica Argentina, 65: 57–65.

Sabbour, M.M. 2014. Biocontrol of the tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. Middle East Journal of Agriculture Research, 3: 499–503.

Sabbour, M.M. & Soliman, N. 2014. Evaluations of three Bacillus thuringiensis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. International Journal of Science and Research, 3: 2067–2073.

Sabino, P.H.S., Sales, F.S., Guevara, E.J., Moino, A. Jr. & Filgueiras, C.C. 2014. Compatibility of entomopathogenic nematodes (Nematoda: Rhabditida) with insecticides used in the tomato crop. Nematoda, 1: e03014. Doi: 10.4322/nematoda.03014

Shannag, H.K., Webb, S.E. & Capinera, J.L. 1994. Entomopathogenic nematode effect on pickleworm (Lepidoptera: Pyralidae) under laboratory and field conditions. Journal of Economic Entomology, 87: 1205–1212.

Sharma, M.P., Sharma, A.N. & Hussaini, S.S. 2011. Entomopathogenic nematodes, a potential microbial biopesticide: Mass production and commercialisation status – a mini review. Archives of Phytopathology and Plant Protection, 44: 855–870.

Smits, P.H., Wiegers, G.L. & Vlug, H.J. 1994. Selection of insect parasitic nematodes for biological control of the garden chafer, Phyllopertha horticola. Entomologia Experimentalis et Applicata, 70: 77–82.

Stock, S.P. & Goodrich-Blair, H. 2012. Nematode parasites, pathogens and associates of insects and invertebrates of economic importance. pp. 373–426. In: Lacey, L.A. (ed.), Manual of Techniques in Insect Pathology. 2nd ed. Academic Press, San Diego.

Terzidis, A.N., Wilcockson, S. & Leifert, C. 2014. The tomato leaf miner (Tuta absoluta): Conventional pest problem, organic management solutions? Organic Agriculture, 4: 43–61.

Tomalak, M., Piggott, S. & Jagdale, G.B. 2005. Glasshouse applications. pp 147–166. In: Grewal, P.S., Ehlers, R-U. & Shapiro-Ilan, D.I. (eds), Nematodes as Biocontrol Agents. CABI Publishing, Oxon.

Urbaneja, A., González-Cabrera, J., Arnó, J. & Gabarra, R. 2012.Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest management Science, 68: 1215–1322.

Urbaneja, A., Desneux, N., Gabarra, R., Arnó, J., González-Cabrera, J., Mafra Neto, A., Stoltman, L., Pinto, A. de S. & Parra, J. R. P. 2013. Biology, ecology and management of the South American tomato pinworm, Tuta absoluta. pp. 98–125. In: Peña, J.E. (ed.), Potential Invasive Pests of Agricultural Crops. CAB International, Wallingford.

Vashisth, S., Chandel, Y.S. & Sharma, P.K. 2013. Entomopathogenic nematodes - A review. Agricultural Reviews, 34: 163–175.

Weiser, J. 1955. Neoplectana carpocapsae n.sp. (Angullulinata: Steinernematidae) novy, cizopasnic housenik obalece jableeneho, Carpocapsa pomonella L. Věstník Československé zoologické společnosti, 19: 44–52.

White, G.F. 1927. A method for obtaining infective nematode larvae from cultures. Science, 66: 302–303.

Wouts, W.M., Mracek, Z., Gerdin, S. & Bedding, R.A. 1982. Neoplectana Steiner, 1929 a junior synonym of Steinernema Travassos, 1927 (Nematoda: Rhabditida). Parasitology, 4: 147–154.

Zappalà, L., Bernardo, U., Biondi, A., Cocco, A., Deliperi, S., Delrio, G., Giorgini, M., Pedata, P., Rapisarda.C., Tropea Garzia, G. & Siscaro, G. 2012a. Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bulletin of Insectology, 65: 51–61.

Zappalà, L., Siscaro, G., Biondi, A., Mollá, O., González-Cabrera, J. & Urbaneja, A. 2012b. Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. Journal of Applied Entomology, 136: 401–409.

References

Abbott, W.S. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18: 265–276.
Abootorabi, E. 2014. Report of native isolate pathogenicity of Steinernema feltiae on tomato leafminer, Tuta absoluta. Biocontrol in Plant Protection, 1: 107–109.
Adams, B.J., Fodor, A., Koppenhöfer, H.S., Stackebrandt, E., Stock, S.P. & Klein, M.G. 2006. Biodiversity and systematics of nematode-bacterium entomopathogens. Biological Control, 37: 32–49.
Arnó, J. & Gabarra, R. 2011. Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). Journal of Pest Science, 84: 513–520.
Arthurs, S., Heinz, K.M. & Prasifka, J.R. 2004. An analysis of using entomopathogenic nematodes against above ground pest. Bulletin of Entomological Research, 94: 297–306.
Batalla-Carrera, L., Morton, A. & García-del-Pino, F. 2010. Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl, 55: 523–530.
Begley, J.W. 1990. Efficacy against insects in habitats others than soil. pp. 215–231. In: Gaugler, R. & Kaya, H.K. (eds.), Entomopathogenic Nematodes in Biological Control. CRC Press, Boca Raton.
Campbell, J.F. & Gaugler, R. 1993. Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Behaviour, 126: 155–169.
Desneux, N., Ramirez-Romero, R. & Kaiser, L. 2006. Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environmental Toxicology and Chemistry, 25: 2675–2682.
Desneux, N., Decourtye, A. & Delpuech, J.M. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81–106.
Desneux, N., Wajnberg, E., Wyckhuys., K.A.G., Burgio., G., Arpaia, S., Narvaez-Vasquez, C.A., Gonzalez-Cabrera, J., Ruescas, D.C., Tabone, E., Frandon, J., Pizzol, J., Poncet, C., Cabello, T. & Urbaneja, A. 2010. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science, 83: 197–215.
Desneux, N., Luna, M.G., Guillemaud, T. & Urbaneja, A. 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. Journal of Pest Science, 84: 403–408.
Divya, K. & Sankar, M. 2009. Entomopathogenic nematodes in pest management. Indian Journal of Science and Technology, 2: 53–60.
Do Thi Khanh, H., Chailleux, A., Tiradon, M., Desneux, N., Colombel, E. & Tabone, E. 2012. Using new egg parasitoids (Trichogramma spp.) to improve integrated management against Tuta absoluta. Bulletin OEPP/EPPO Bulletin, 42: 249–254.
Dowds, B.C.A. & Peters, A. 2002. Virulence mechanisms. pp. 79–98. In: Gaugle, R. (ed.), Entomopathogenic Nematology. CAB International, Wallingford.
Ebssa, L. & Koppenhöfer, A.M. 2012. Entomopathogenic nematodes for the management of Agrotis ipsilon: effect of instar, nematode species and nematode production method. Pest Management Science, 68: 947–957.
Ehlers, R.U. & Shapiro-Ilan, D.I. 2005. Mass production. pp. 65–78. In: Grewal, P.S., Ehlers, R.U. & Shapiro-Ilan, D.I. (eds.), Nematodes as Biocontrol Agents. CAB International, Wallingford.
Gabarra, R., Arnó, J., Lara, L., Verdú, M.J., Ribes, A., Beitia, F., Urbaneja, A., Téllez, M. Del M., Mollá, O. & Riudavets, J. 2014. Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast. Biocontrol, 59: 45–54.
Garcia-del-Pino, F., Alabern, X. & Morton, A. 2013. Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl, 58: 723–731.
Ghoneim, K. 2014. Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. Journal of Entomology and Zoology Studies, 2: 52–71.
Griffin, C.T., Boemare, N.E. & Lewis, E.E. 2005. Biology and behavior. pp. 47–64. In: Grewal, P.S., Ehlers, R.U. & Shapiro-Ilan, D.I. (eds.), Nematodes as Biocontrol Agents. CAB International, Wallingford.
Hallem, E.A., Dillman, A.R., Hong, A.V., Zhang, Y., Yano, J.M., DeMarco, S.F. & Sternberg, P.W. 2011. A sensory code for host seeking in parasitic nematodes. Current Biology, 21: 377–383.
Hominick, W.M. 2002. Biogeography. pp. 115–143. In: Gaugler, R. (ed.), Entomopathogenic Nematology. CABI Publishing, Wallingford.
Hunt, D.J. 2007. Introduction. pp. 1–26. In: Nguyen, K.B. & Hunt, D.J. (eds.), Hunt, D.J. & Perry, R.N. (Series eds.), Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts, Nematology Monographs and Perspectives. Koninklijke Brill NV, Leiden.
Jackson, J.J. & Brooks, M.A. 1995. Parasitism of western corn rootworm larvae and pupae by Steinernema carpocapsae. Nematology, 27: 15–20.
Kaya, H.K. & Stock, S.P. 1997. Techniques in insect nematology. pp. 281–324. In: Lacey, L. (ed.), Manual of Techniques in Insect Pathology. Academic Press, San Diego.
Kim, H.H., Choo, H.Y., Kaya, H.K., Lee, D.W., Lee, S.M. & Jeon, H.Y. 2004. Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biological control agent against the fungus Gnat Bradysia agrestis (Diptera: Sciaridae) in propagation houses. Biocontrol Science and Technology, 14: 171–183.
Koppenhöfer, A.M. 2000. Nematodes. pp. 283–301. In: Lacey, L.A. & Kaya, H.K. (eds.), Field Manual of Techniques in Invertebrate Pathology. Kluwer, Dordrecht.
Koppenhöfer, A.M. & Kaya, H.K. 2002. Entomopathogenic nematodes and insect pest management. pp. 258–313. In: Koul, O. & Dhaliwal, G.S. (eds.) Microbial Biopesticides. Taylor & Francis, Abingdon.
Lacey, L.A. & Georgis, R. 2012. Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. Journal of Nematology, 44: 218–225.
Lewis, E.E. 2002. Behavioural ecology. pp. 205–223. In: Gaugle, R. (ed.) Entomopathogenic Nematology, CAB International, Wallingford.
Lewis, E.E., Gaugler, R. & Harrison, R. 1993. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Canadian Journal of Zoology, 71: 765–769.
Lewis, E.E., Grewal, P.S. & Gaugler, R. 1995. Hierarchical order of host cues in parasite foraging strategies. Parasitology, 110: 207–213.
Lietti, M.M.M., Botto, E. & Alzogaray, P.A. 2005. Insecticide Resistance in Argentine Populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology, 34:113–119.
Metwally, H.M.S., Hafez, G.A., Hussein, M.A., Hussein, M.A., Salem, H.A. & Saleh, M.M.E. 2012. Low cost artificial diet for rearing the greater wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae) as a host for entomopathogenic nematodes. Egyptian Journal of Biological Pest Control, 22: 15–17.
Moosavi, M.R. & Zare, R. 2012. Fungi as biological control agents of plant-parasitic nematodes. pp: 67–107. In: Merillon, J.M. & Ramawat, K.G. (eds.), Plant Defence: Biological Control, Progress in Biological Control 12. Springer Science + Business Media, Dordrecht.
Moosavi, M.R. & Askary, T.H. 2015. Nematophagous fungi- Commercialization. pp: 187–202. In: Askary, T.H. & Martinelli, P.R.P. (eds.), Biocontrol Agents of Phytonematodes. CABI Publishing, Wallingford.
Nannini, M., Atzori, F., Murgia, G., Pisci, R. & Sanna, F. 2012. Use of predatory mirids for control of the tomato borer Tuta absoluta (Meyrick) in Sardinian greenhouse tomatoes. Bulletin OEPP/EPPO Bulletin, 42: 255–259.
Nguyen, K.B. 2007. Methodology, morphology and identification. pp. 59–119. In: Nguyen, K.B. & Hunt, D.J. (eds.) Hunt, D.J. & Perry, R.N. (series eds.), Entomopathogenic Nematodes: Systematics, Phylogeny and Bacterial Symbionts, Nematology Monographs and Perspectives. Koninklijke Brill NV, Leiden.
Poinar, G.O. Jr. 1976. Description and biology of a new insect parasitic rhabditoid, Heterorhabditis bacteriophora n. gen., n. sp. (Rhabditida: Heterorhabditidae n. fam.). Nematologica, 21:463–470.
Půža, V. 2015. Control of insect pests by entomopathogenic nematodes. pp. 175–183. In: Lugtenberg, B. (ed.), Principles of Plant-Microbe Interaction. Springer International Publishing, Bern.
Riquelme, V.M., Botto, E.N. & Lafalce, C. 2006. Efficacy of insecticides against the “Tomato moth”, Tuta absoluta (Lepidoptera: Gelechiidae) and their residual effects on the parasitoid Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae). Revista de la Sociedad Entomológica Argentina, 65: 57–65.
Sabbour, M.M. 2014. Biocontrol of the tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. Middle East Journal of Agriculture Research, 3: 499–503.
Sabbour, M.M. & Soliman, N. 2014. Evaluations of three Bacillus thuringiensis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. International Journal of Science and Research, 3: 2067–2073.
Sabino, P.H.S., Sales, F.S., Guevara, E.J., Moino, A. Jr. & Filgueiras, C.C. 2014. Compatibility of entomopathogenic nematodes (Nematoda: Rhabditida) with insecticides used in the tomato crop. Nematoda, 1: e03014. doi: 10.4322/nematoda.03014
Shannag, H.K., Webb, S.E. & Capinera, J.L. 1994. Entomopathogenic nematode effect on pickleworm (Lepidoptera: Pyralidae) under laboratory and field conditions. Journal of Economic Entomology, 87: 1205–1212.
Sharma, M.P., Sharma, A.N. & Hussaini, S.S. 2011. Entomopathogenic nematodes, a potential microbial biopesticide: Mass production and commercialisation status – a mini review. Archives of Phytopathology and Plant Protection, 44: 855–870.
Smits, P.H., Wiegers, G.L. & Vlug, H.J. 1994. Selection of insect parasitic nematodes for biological control of the garden chafer, Phyllopertha horticola. Entomologia Experimentalis et Applicata, 70: 77–82.
Stock, S.P. & Goodrich-Blair, H. 2012. Nematode parasites, pathogens and associates of insects and invertebrates of economic importance. pp. 373–426. In: Lacey, L.A. (ed.), Manual of Techniques in Insect Pathology. 2nd ed. Academic Press, San Diego.
Terzidis, A.N., Wilcockson, S. & Leifert, C. 2014. The tomato leaf miner (Tuta absoluta): Conventional pest problem, organic management solutions? Organic Agriculture, 4: 43–61.
Tomalak, M., Piggott, S. & Jagdale, G.B. 2005. Glasshouse applications. pp 147–166. In: Grewal, P.S., Ehlers, R-U. & Shapiro-Ilan, D.I. (eds) Nematodes as Biocontrol Agents. CABI Publishing, Oxon.
Urbaneja, A., González-Cabrera, J., Arnó, J. & Gabarra, R. 2012.Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest management Science, 68: 1215–1322.
Urbaneja, A., Desneux, N., Gabarra, R., Arnó, J., González-Cabrera, J., Mafra Neto, A., Stoltman, L., Pinto, A. de S. & Parra, J. R. P. 2013. Biology, ecology and management of the South American tomato pinworm, Tuta absoluta. pp. 98–125. In: Peña, J.E. (ed.), Potential Invasive Pests of Agricultural Crops. CAB International, Wallingford.
Vashisth, S., Chandel, Y.S. & Sharma, P.K. 2013. Entomopathogenic nematodes - A review. Agricultural Reviews, 34: 163–175.
Weiser, J. 1955. Neoplectana carpocapsae n.sp. (Angullulinata: Steinernematidae) novy, cizopasnic housenik obalece jableeneho, Carpocapsa pomonella L. Věstník Československé zoologické společnosti, 19: 44–52.
White, G.F. 1927. A method for obtaining infective nematode larvae from cultures. Science, 66: 302–303.
Wouts, W.M., Mracek, Z., Gerdin, S. & Bedding, R.A. 1982. Neoplectana Steiner, 1929 a junior synonym of Steinernema Travassos, 1927 (Nematoda: Rhabditida). Parasitology, 4: 147–154.
Zappalà, L., Bernardo, U., Biondi, A., Cocco, A., Deliperi, S., Delrio, G., Giorgini, M., Pedata, P., Rapisarda.C., Tropea Garzia, G. & Siscaro, G. 2012a. Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bulletin of Insectology, 65: 51–61.
Zappalà, L., Siscaro, G., Biondi, A., Mollá, O., González-Cabrera, J. & Urbaneja, A. 2012b. Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. Journal of Applied Entomology, 136: 401–409.

Files

Share

How to cite

Statistics