Skip to main content

Environmental Impacts of Entomopathogenic Nematodes Used for Biological Control in Soil

  • Chapter
Book cover Nontarget Effects of Biological Control

Abstract

Biological control is a powerful tactic that has been used to obtain many significant, well documented economic and public health benefits against pests in agroecosystems and against disease vectors (Caltagirone 1981, DeBach 1974, Pimentel et al. 1984). The use of biological control has generally been considered environmentally safe and risk-free (Batra 1982, DeBach 1974, Hokkanen and Pimentel 1989, Hoy 1992), especially in comparison to the widespread use of synthetic insecticides (Pedigo and Higley 1992, Pimentel et al. 1992). However, data to support the assumption of absence of environmental impacts are not regularly collected (Howarth 1991), and it cannot be assumed that the lack of published evidence of negative environmental impacts is evidence of their absence. Indications of the growing concern about this complex issue include the recent debate in the literature over the use of introduced biological control agents to manage rangeland grasshoppers (Carruthers and Onsager 1993, Lockwood 1993a, b).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akhurst, R. J. 1990. Safety to nontarget invertebrates of nematodes of economically important pests. In M. Laird, L. A. Lacey, and E. W. Davidson (eds.), Safety of microbial insecticides. CRC Press, Boca Raton, Florida. p. 233–240.

    Google Scholar 

  • Akhurst, R. J., and R. A. Bedding. 1986. Natural occurrence of insect pathogenic nematodes (Steinernematida and Heterorhabditidae) in soil in Australia. J. Aust. Entomol. Soc. 25: 241

    Article  Google Scholar 

  • Akhurst, R. J., R. A. Bedding, R. M. Bull, and D. R. J. Smith. 1992. An epizootic of Hetewrhabditis sp. (Heterorhabditidae: Nematoda) in sugar cane Scarabaeidae (Coleoptera). Fundam. Appl. Nematol. 15: 71–73.

    Google Scholar 

  • Akhurst, R. J., and N. E. Boemare. 1990. Biology and taxonomy of Xenorhabdus. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida. p. 75–90.

    Google Scholar 

  • Akhurst, R. J., and W. M. Brooks. 1984. The distribution of entomophilic nematodes (Heterorhabditidae and Steinernematidae) in North Carolina. J. Invertebr. Pathol. 44: 140–145.

    Article  Google Scholar 

  • Alatorre-Rosas, R., and H. K. Kaya. 1990. Interspecific competition between entomopathogenic nematodes in the genera Hetewrhabditis and Steinernema for an insect host in sand. J. Invertebr. Pathol. 55: 179–188.

    Article  Google Scholar 

  • Alatorre-Rosas, R., and H. K. Kaya. 1991. Interaction between two entomopathogenic nematode species in the same host. J. Invertebr. Pathol. 57: 1–6.

    Article  Google Scholar 

  • Baker, K. F., and R. J. Cook. 1974. Biological control of plant pathogens. W. H. Freeman, San Francisco. 433p.

    Google Scholar 

  • Barbercheck, M. E., and H. K. Kaya. 1990. Interactions between Beauveria bassiana and the entomogenous nematodes, Steinernema feltiae and Heterorhabditis heliothidis. J. Invertebr. Pathol. 55: 225–234.

    Article  Google Scholar 

  • Barbercheck, M. E., and H. K. Kaya. 1991a. Effect of host condition and soil texture on host finding by the entomogenous nematodes Heterorhabditis bacteriophora (Rhabditida:Heterorhabditidae) and Steinernema carpocapsae (Rhabditida: Steinernematidae). Environ. Entomol. 20:582–589.

    Google Scholar 

  • Barbercheck, M. E., and H. K. Kaya. 1991b. Competitive interactions between entomopathogenic nematodes and Beauveria bassiana (Deuteromycotina: Hyphomycetes) in soilborne larvae of Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 20: 707–712.

    Google Scholar 

  • Barbercheck, M. E. 1992. Effect of soil physical factors on biological control agents of soil insect pests. Florida Entomol. 75:539–548.

    Article  Google Scholar 

  • Barbercheck, M. E. 1993. Tritrophic level effects on entomopathogenic nematodes. Environ. Entomol. 22: 1166–1171.

    Google Scholar 

  • Barbercheck, M. E., J. Wang, and I. S. Hirsh. 1995. Host plant effects on entomopathogenic nematodes. J. Invertebr. Pathol. 66: 169–177.

    Article  Google Scholar 

  • Bathon, H. 1996. Impact of entomopathogenic nematodes on non-target hosts. Biocontrol Sci. Tech. 6: 421–434.

    Article  Google Scholar 

  • Batra, S. W. T. 1982. Biological control in agroecosystems. Science 215: 134–139.

    Article  PubMed  CAS  Google Scholar 

  • Beavers, J. B., C. W. McCoy, and D. T. Kaplan. 1983. Natural enemies of subterranean Diaprepes abbreviates (Coleoptera: Curculionidae) larvae in Florida. Environ. Entomol. 12: 840–843.

    Google Scholar 

  • Bedding, R. A., and R. J. Akhurst. 1975. A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21: 109–110.

    Article  Google Scholar 

  • Bedding, R. A., and A. S. Molyneux. 1982. Penetration of insect cuticle by infective juveniles of Heterorhabditis sp. (Heterorhabditidae: Nematoda). Nematologica 28: 354–359.

    Article  Google Scholar 

  • Bedding, R. A., A. S. Molyneux, and R. J. Akhurst. 1983. Heterorhabditis sp., Neoaplectana sp., and Steinernema kraussei. interspecific and intraspecific differences in infectivity for insects. Exp. Parasitol, 55:249–257.

    Article  PubMed  CAS  Google Scholar 

  • Bednarek, A., and T. Nowicki. 1986. New estimation method for the density of entomogenous nematodes (Rhabditidae: Steinernematidae) in the soil. Rev. Nematol. 14: 638–39.

    Google Scholar 

  • Bennett, F. D. 1993. Do introduced parasitoids displace native ones? Florida Entomol. 76: 54–63.

    Article  Google Scholar 

  • Bird, A. F., and J. Bird. 1986. Observations on the use of insect parasitic nematodes as a means of biological control of root-knot nematodes. Int. J. Parasitol. 16: 511–516.

    Article  Google Scholar 

  • Boemare, N. E., R. J. Akhurst, and R. G. Mourant. 1993. DNA relatedness between Xenorhabdus sp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. nov. Int. J. Syst. Bacteriol. 43: 249–255.

    Article  CAS  Google Scholar 

  • Boemare, N., C. Laumond, and H. Mauleon. 1996. The entomopathogenic nematode-bacterium complex: biology, life cycle and vertebrate safety. Biocontrol Sci. Tech. 6: 333–345.

    Article  Google Scholar 

  • Bohan, D. A., and W. M. Hominick. 1995. Intra-population infectious structure and temporal variation in Steinernema feltiae. In C. T. Griffen, R. L. Gwynn and J. P. Masson (eds.), Ecology and transmission strategies of entomopathogenic nematodes. European Commission, Luxembourg. p. 83–94.

    Google Scholar 

  • Brust, G. E. 1991. Augmentation of an endemic entomogenous nematode by agroecosystem manipulation for the control of a soil pest. Agric. Ecosyst. Environ. 36: 175–184.

    Article  Google Scholar 

  • Buck, M., and H. Bathon. 1993. Auswirkungen des Einsatzes entomopathogener Nematoden (Heterorhabditis sp.) im Freiland auf die Nichtzielfauna, 2. Teil: Diptera. Anzeiger für Schadlingskunde, Pflanzenschutz, Umweltschutz 66: 84–88

    Article  Google Scholar 

  • Burges, H. D., and N. W. Hussey. 1971. Microbial control of insects and mites. Academic Press, New York.

    Google Scholar 

  • Cabanillas, H. E., and J. R. Raulston. 1994. Evaluation of the spatial pattern of Steinernema riobravis in corn plots. J. Nematol. 26: 25–31.

    PubMed  CAS  Google Scholar 

  • Caltagirone, L. E. 1981. Landmark examples in classical biological control. Annu. Rev. Entomol. 26: 213–232.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Campbell, J. F., E. Lewis, F. Yoder, and R. Gaugler. 1995. Entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) seasonal population dynamics and impact on insect populations in turfgrass. Biol. Control 5: 598–606.

    Article  Google Scholar 

  • Carruthers, R. I., and J. A. Onsager. 1993. Perspective on use of exotic natural enemies for biological control of pest grasshoppers (Orthoptera: Acrididae). Environ. Entomol. 22: 885–903.

    Google Scholar 

  • Cohen, J. E., R. A. Beaver, S. H. Cousins, D. L. DeAngelis, L. Goldwasser, K. L. Heong, R. D. Holt, A. J. Kohn, J. H. Lawton, N. Martinez, R. O’Malley, L. M. Page, B. C. Patten, S. L. Pimm, G. A. Polis, M. Rejmanek, T. W. Schoener, K. Schoenly, W. G. Sprules, J. M. Teal, R. E. Ulanowicz, P. H. Warren, H. M. Wilbur, and P. Yodzis. 1993. Improving food webs. Ecology 74: 252–258.

    Article  Google Scholar 

  • DeBach. P. 1974. Biological control by natural enemies. London: Cambridge Univ. Press. 323 p.

    Google Scholar 

  • Downes, M. J., and C. T. Griffin. 1996. Dispersal behaviour and transmission strategies of the entomopathogenic nematodes Heterorhabditis and Steinernema. Biocontrol Sci. Technol. 6: 347–356.

    Article  Google Scholar 

  • Ehlers, R.-U., K. V. Deseo, and E. Strackebrandt. 1991. Identification of Steinernema sp. (Nematoda) and their symbiotic bacteria Xenorhabdus sp. from Italian and German soils. Nematologica 37:360–366.

    Article  Google Scholar 

  • Ehlers, R.-U., and A. Peters. 1995. Entomopathogenic nematodes in biological control: feasibility, perspectives and possible risks. In H. M. T. Hokkanen and J. M. Lynch (eds.), Biological control: benefits and risks. Cambridge Univ. Press. p. 119–136.

    Google Scholar 

  • Ehlers, R.-U., and H. M. T. Hokkanen. 1996. Insect biocontrol with non-endemic entomopathogenic nematodes (Steinernema and Heterorhabditis sp.): OECD and COST workshop on scientific and regulatory policy issues. Biocontrol Sci. Tech. 6: 295–302.

    Article  Google Scholar 

  • Epsky, N. D., and J. L. Capinera. 1993. Quantification of invasion of two strains of Steinernama carpocapsae (Weiser) into three lepidopteran larvae. J. Nematol. 25:173–180.

    PubMed  CAS  Google Scholar 

  • Epsky, N. D., D. E. Walter, and J. L. Capinera. 1988. Potential role of nematophagous microarthropods as biotic mortality factors of entomopathogenic nematodes (Rhabditida, Steinernematidae and Heterorhabditidae). J. Econ. Entomol. 81: 821–825.

    Google Scholar 

  • Fan, X., and W. M. Hominick. 1991. Efficiency of Galleria (wax moth baiting technique for recovering infective stage of entomopathogenic rhabditids (Steinernematidae and Heterorhabditidae) from sand and soil. Revue de Nematol. 14:381–387.

    Google Scholar 

  • Fleming, W. E. 1968. Biological control of the Japanese beetle. USDA Tech. Bull. No. 1383. 78 p.

    Google Scholar 

  • Fuxa, J. R. 1987. Ecological considerations for the use of entomopathogens in IPM. Annu. Rev. Entomol. 32: 225–251.

    Article  Google Scholar 

  • Gaugier, R. 1988. Ecological considerations in the biological control of soil-inhabiting insects with entomopathogenic nematodes. Agric. Ecosyst. Environ. 24: 361–60.

    Article  Google Scholar 

  • Gaugler, R., and G. M. Boush. 1979. Nonsusceptibility to rats to the entomopathogenic nematode, Neoaplectana carpocapsae. Environ. Entomol. 8: 658–660.

    Google Scholar 

  • Gaugler, R., and H. K. Kaya. 1990. Entomopathogenic nematodes in biological control. CRC, Boca Raton. 365 p.

    Google Scholar 

  • Gaugler, R., J. F. Campbell, and T. R. McGuire. 1989a. Selection for host-finding in Steinernema feltiae. J. Invertebr. Pathol. 54: 363–372.

    Article  Google Scholar 

  • Gaugler, R., J. F. Campbell, and P. Gupta. 1991. Characterization and basis of enhanced host-finding in a genetically improved strain of Steinernema carpocapsae. J. Invertebr. Pathol. 57: 234–241.

    Article  Google Scholar 

  • Gaugler, R., J. F. Campbell, S. Selvan, and E. E. Lewis. 1992. Large-scale inoculative releases of the entomopathogenic nematode Steinernema glasen. Assessment 50 years later. Biol. Control 2: 181–187.

    Article  Google Scholar 

  • Gaugler, R., T. McGuire, and J. Campbell. 1989b. Genetic variability among strains of the entomopathogenic nematode Steinernema feltiae. J. Nematol. 21: 247–253.

    PubMed  CAS  Google Scholar 

  • Gaugler, R., and D. Molloy. 1981. Instar susceptibility of Simulium vittatum (Diptera: Simuliidae) to the entomogenous nematode Neoaplectana carpocapsae. J. Nematol. 13: 1–5.

    PubMed  CAS  Google Scholar 

  • Geden, C. J., R. C. Axtell, and W. M. Brooks. 1985. Susceptibility of the lesser mealworm Aliphitobius diaperinus (Coleoptera: Tenebrionidae) to the entomogenous nematodes Steinernema feltiae, S. glaseri (Steinernematidae) and Heterorhabditis heliothidis (Heterorhabditidae). J. Entomol. Sci. 20: 331–339.

    Google Scholar 

  • Georgis, R. 1992. Present and future prospects for entomopathogenic nematode products. Biocontrol Sci. Tech. 2: 83–99.

    Article  Google Scholar 

  • Georgis, R., and R. Gaugler. 1991. Predictability in biological control using entomopathogenic nematodes. J. Econ. Entomol. 84: 713–720.

    Google Scholar 

  • Georgis, R., and N. G. M. Hague. 1981. Field evaluation of Steinernema feltiae against the web-spinning larch sawfly Cephalia lariciphila. J. Nematol. 20: 317–320.

    Google Scholar 

  • Georgis, R., and G. O. Poinar, Jr. 1983a. Effect of soil texture on the distribution and infectivity of Neoaplectana carpocapse (Nematoda: Steinernematidae). J. Nematol. 15: 308–311.

    PubMed  CAS  Google Scholar 

  • Georgis, R., and G. O. Poinar, Jr. 1983b. Effect of soil texture on the distribution and infectivity of Neoaplectana glaseri (Nematoda: Steinernematidae). J. Nematol. 15: 329–332.

    PubMed  CAS  Google Scholar 

  • Georgis, R., and G. O. Poinar, Jr. 1983c. Effect of soil texture on the distribution and infectivity of Heterorhabditis heliothidis (Nematoda: Steinernematidae). J. Nematol. 15: 652–654.

    PubMed  CAS  Google Scholar 

  • Georgis, R., H. K. Kaya, and R. Gaugler. 1991. Effect of steinernematid and heterorhabditid nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on nontarget arthropods. Environ. Entomol. 20: 815–822.

    Google Scholar 

  • Gilmore, S. K., and D. A. Potter. 1993. Potential role of Collembola as biotic mortality agents for entomopathogenic nematodes. Pedobiologia 37: 30–38.

    Google Scholar 

  • Gilmore, S. K., and E. M. Raffensperger. 1970. Foods ingested by Tomocerus sp. [Collembola, Entomobryidae], in relation to habitat. Pedobiologia 10: 135–140.

    Google Scholar 

  • Glazer, I., R. Gaugler, and D. Segal. 1991. Genetics of the nematode Heterorhabditis bacteriophora strain HP88: The diversity of beneficial traits. J. Nematol. 23:324–333.

    PubMed  CAS  Google Scholar 

  • Götz, P., A. Boman, and H. G. Boman. 1981. Interactions between insect immunity and an insect pathogenic nematode with symbiotic bacteria. Proc. R. Soc. London, Ser. B. 212:333–350.

    Article  Google Scholar 

  • Grewal, P. S., E. E. Lewis, R. Gaugler, and J. F. Campbell. 1994. Host finding behaviour as a predictor for foraging strategy for entomopathogenic nematodes. Parasitology 108: 207–215.

    Article  Google Scholar 

  • Grewal, P. S., R. Gaugler, and R. Georgis. 1995. Predictors of foraging strategy in entomopathogenic nematodes. In C. T. Griffen, R. L. Gwynn, and J. P. Masson (eds.), Ecology and transmission strategies of entomopathogenic nematodes. European Commission, Luxembourg. p. 95–104.

    Google Scholar 

  • Grewal. p. S., W. R. Martin, R. W. Miller, and E. E. Lewis. 1997. Suppression of plant-parasitic nematode populations in turfgrass by application of entomopathogenic nematodes. Biocontrol Sci. Technol. 7: 393–399.

    Article  Google Scholar 

  • Griffin, C. T., W. R. Simons, and P. H. Smits. 1989. Activity and infectivity of four isolates of Heterorhabditis sp. J. Invertebr. Pathol. 53: 107–112.

    Article  Google Scholar 

  • Griffin, C. T., J. F. Moore, and M. J. Downes. 1991. Occurrence of insect-parasitic nematodes (Steinernematidae, Heterorhabditidae) in the Republic of Ireland. Nematologica 37: 92–100.

    Article  Google Scholar 

  • Griffin, C. T., S. A. Joyce, I. Dix, A. M. Burnell, and M. J. Downes. 1994. Characterisation of the entomopathogenic nematode Heterorhabditis (Nematoda: Heterorhabditidae) from Ireland and Britain by molecular and cross-breeding techniques, and the occurrence of the genus in these islands. Fund. Appl. Nematol. 17: 245–254.

    Google Scholar 

  • Han, R., W. M. Wouts, and L. Li. 1991. Development and virulence of Heterorhabditis sp. strains associated with different Xenorhabdus luminescens isolates. J. Invertebr. Pathol. 58:27–32.

    Article  Google Scholar 

  • Hara, A. H., R. Gaugler, H. K. Kaya, and L. M. LeBeck. 1991. Natural populations of entomopathogenic nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) from the Hawaiian Islands. Environ. Entomol. 20: 211–216.

    Google Scholar 

  • Harris. p. 1990. Environmental impact of introduced biological control agents. In M. Mackauer, L. E. Ehler and J. Roland (eds.), Critical issues in biological control. Intercept, Andover. p. 289–300.

    Google Scholar 

  • Hawksworth, D. L. 1991. The biodiversity of microorganisms and invertebrates: Its role in sustainable agriculture. CAB International, Oxon, UK. 302 p.

    Google Scholar 

  • Hokkanen, H. M. T., and D. Pimentel. 1989. New associations in biological control: theory and practice. Can. Entomol. 121 829–840.

    Article  Google Scholar 

  • Hokkanen, H. M. T., and J. M. Lynch. 1995. Biological control: Benefits and risks. Cambridge Univ. Press. 304 p.

    Google Scholar 

  • Hominick, W. M., and B. R. Briscoe. 1990. Occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in British soils. Parasitology 100: 295–302.

    Article  Google Scholar 

  • Hominick, W. M., and A. P. Reid. 1990. Perspectives on entomopathogenic nematology. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida. p. 327–345.

    Google Scholar 

  • Hominick, W. M., A. P. Reid, D. A. Bohan, and B. R. Briscoe. 1996. Entomopathogenic nematodes: biodiversity, geographical distribution and the Convention on Biological Diversity. Biocontrol Sci. Technol. 6: 317–331.

    Article  Google Scholar 

  • Howarth, F. G. 1991. Environmental impacts of classical biological control. Annu. Rev. Entomol. 36: 485–509.

    Article  Google Scholar 

  • Hoy, M. A. 1992. Biological control of arthropods: genetic engineering and environmental risks. Biol. Control 2: 166–170.

    Article  Google Scholar 

  • Ishibashi, N., and E. Kondo. 1986. Steinernema feltiae (DD-136) and S. glaseri: persistence in soil and bark compost and their influence on native nematodes. J. Nematol. 18: 310–316.

    PubMed  CAS  Google Scholar 

  • Ishibashi, N., and E. Kondo. 1987. Dynamics of the entomogenous nematode Steinernema feltiae applied to soil with and without nematicide treatment. J. Nematol. 19: 404–412.

    PubMed  CAS  Google Scholar 

  • Ishibashi, N., and E. Kondo. 1990. Behavior of infective juveniles. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic nematodes in biological control. CRC, Boca Raton, Florida. p. 139–150.

    Google Scholar 

  • Ives, R. A., and R. M. May. 1985. Competition within and between species in a patchy environment: Relations between microscopic and macroscopic models. J. Theor. Biol. 115:65–92.

    Article  Google Scholar 

  • Jackson, J. J., and M. A. Brooks. 1989. Susceptibility and immune response of western corn rootworm larvae (Coleoptera: Chrysomelidae) to the entomogenous nematode, Steinernema feltiae (Rhabditida: Steinernematidae). J. Econ. Entomol. 82: 1073–1077.

    Google Scholar 

  • Jackson, T. A., and W. M. Wouts. 1987. Delayed action of an entomopathogenic nematode Heterorhabditis sp. (V16) for grass grub control. Proc. 40th New Zealand Weed and Pest Control Conf: 3–35.

    Google Scholar 

  • Jansson, R. K. 1993. Introduction of exotic entomopathogenic nematodes (Rhabditida: Heterorhabditida and Steinernematidae) for biological control of insects: potential and problems. Florida Entomol. 76: 82–96.

    Article  Google Scholar 

  • Jansson, R. K., S. H. Lecrone, and R. Gaugler. 1991. Comparison of single and multiple releases of Heterorhabditis bacteriophora Poinar (Nematoda: Heterorhabditidae) for control of Cylas formicarius (Fabricius) (Coleoptera Apionidae). Biol. Control 1:320–328.

    Article  Google Scholar 

  • Jansson, R. K., S. H. Lecrone, and R. Gaugler. 1993. Field efficacy and persistence of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) as biological control agents of the sweetpotato weevil (Coleoptera: Apionidae) in southern Florida. J. Econ. Entomol. 86: 1055–1063.

    Google Scholar 

  • Kaya, H. K. 1978. Interaction between Neoaplectana carpocapsae (Nematoda: Steinernematidae) and Apanteles militaris (Hymenoptera: Braconidae), a parasitoid of the armyworm, Pseudaletia unipuncta. J. Invertebr. Pathol. 31: 358–364.

    Article  Google Scholar 

  • Kaya, H. K., and R. Gaugler. 1993. Entomopathogenic nematodes. Ann Rev. Entomol. 38:181–206.

    Article  Google Scholar 

  • Kaya, H. K., and P. G. Hotchkin. 1981. The nematode Neoaplectana carpocapsae Weiser and its effect on selected ichneumonid and braconid parasites. Environ. Entomol. 10: 474–478.

    Google Scholar 

  • Kaya, H. K. J. Marston, J. Lindegren, and Y. Peng. 1982. Low susceptibility of the honey bee, Apis mellifera L. (Hymenoptera: Apidae) to the entomophagous nematode, Neoaplectana carpocapsae Weiser. Environ. Entomol. 11:920–923.

    Google Scholar 

  • Kermarrec, A., H. Mauleon, C. Sirjusingh, and L. Baud. 1991. Etudes experimentale de la sensibilite de vertebres heterothermes tropicaux (crapauds, grenouilles, lezards) a diverses souches de nematodes entomoparasites des genres Heterorhabditis et Steinernema. Rencontres de Lutte Biologique: 58: 193–204.

    Google Scholar 

  • Kerry, B. 1995. The potential impact of natural enemies on the survival and efficacy of entomopathogenic nematodes. In C.T. Griffin, R. L. Gwynn, and J. P. Masson, (eds.), COST 819 Biotechnology: ecology and transmission strategies of entomopathogenic nematodes, European Commission, Luxembourg. p. 7–13.

    Google Scholar 

  • Klein, M. G. 1990. Efficacy against soil-inhabiting insect pests. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida. p. 195–214.

    Google Scholar 

  • Koch, U., and H. Bathon. 1993. Auswirkungen des Einsatzes entomopathogener Nematoden im Freiland auf die Nichtzielfauna, 1. Teil: Coleoptera. Anzeiger für Schadlingskunde, Pflanzenschutz, Umweltschutz 66: 65–68.

    Article  Google Scholar 

  • Koppenhöfer, A. M., H. K. Kaya, S. Shanmugam, and G. L. Wood. 1995a. Interspecific competition between steinernematid nematodes within an insect host. J. Invertebr. Pathol. 66: 99–103.

    Article  Google Scholar 

  • Koppenhöfer, A. M., H. K. Kaya, and S. Taormino. 1995b. Infectivity of entomopathogenic nematodes (Rhabditida: Steinernematidae) at different soil depths and moistures. J. Invertebr. Pathol. 65:193–199.

    Article  Google Scholar 

  • Koppenhöfer, A. M., and H. K. Kaya. 1996. Coexistence of two steinernematid nematode species (Rhabditida: Steinernematidae) in the presence of two host species. Appl. Soil Ecol. 4: 221–230.

    Article  Google Scholar 

  • Lewis, E. E., R. Gaugler, and R. Harrison. 1992. Entomopathogenic nematode host finding: response to contact cues by by cruise and ambush foragers. Parasitology 105: 309–315.

    Article  Google Scholar 

  • Lewis, E. E., R. Gaugler, and R. Harrison. 1993. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can. J. Zool. 71: 765–769.

    Article  Google Scholar 

  • Lockwood, J. A. 1993a. Environmental issues involved in biological control of rangeland grasshoppers (Orthoptera: Acrididae) with exotic agents. Environ. Entomol. 22: 505–518.

    Google Scholar 

  • Lockwood, J. A. 1993b. Benefits and costs of controlling rangeland grasshoppers (Orthoptera: Acrididae) with exotic organisms: Search for a null hypothesis and regulatory compromise. Environ. Entomol. 22: 904–914.

    Google Scholar 

  • Mannion, C. M., and R. K. Jansson. 1992a. Comparison of ten entomopathogenic nematodes for control of sweetpotato weevil (Coleoptera: Apionidae). J. Econ. Entomol. 85: 1642–1650.

    Google Scholar 

  • Mannion, C. M., and R. K. Jansson. 1992b. Movement and postinfection emergence of entomopathogenic nematodes from sweetpotato weevil, Cylas formicarius (F.) (Coleoptera: Apionidae). Biol. Control 2:297–305.

    Article  Google Scholar 

  • Molyneux, A. S., R. A. Bedding, and R. J. Akhurst. 1983. Susceptibility of larvae of the sheep blowfly, Lucilia cuprina, to various Heterorhabditis sp., Neoaplectana sp., and an undescribed steinernematid (Nematoda). J. Invertebr. Pathol. 42:1–7.

    Article  PubMed  CAS  Google Scholar 

  • Moore, J. C., D. E. Walter, and H. W. Hunt. 1988. Arthropod regulation of micro-and mesobiota in below-ground detrital food webs. Annu. Rev. Entomol. 33: 419–439.

    Article  Google Scholar 

  • Mracek, Z. 1980. The use of “Galleria traps” for obtaining nematode parasites of insects in Czechoslovakia (Lepidoptera: Nematoda, Steinernematidae). Acta ent. bohemoslavica 77: 378–382.

    Google Scholar 

  • Mracek, Z. 1982. Horizontal distribution in soil and seasona dynamics of the nematode Steinernema kraussei, a parasite of Cephalcia abietis. J. Appl. Entomol. 94:110–112.

    Google Scholar 

  • Mracek, Z. 1986. Nematodes and other factors controlling the sawfly, Cephalcia abietis (Pamphilidae: Hymenoptera), in Czechoslovakia. Forest Ecol. Mgt. 15: 75–79.

    Article  Google Scholar 

  • Mueller, B. R., M. H. Beare, and D. A. Crossley. 1990. Soil mites in detrital food webs of conventional and no-tillage agroecosystems. Pedobiologia 34: 389–401.

    Google Scholar 

  • Murphy, P. W., and C. C. Doncaster. 1957. A culture method for soil meiofauna and its application to the study of nematode predators. Nematologica 2: 202–214.

    Article  Google Scholar 

  • Obendorf, D. L., B. Peel, R. J. Akhurst, and L. A. Miller. 1983. Non-susceptibility of mammals to the entomopathogenic bacterium Xenorhabdus nematophilus. Environ. Entomol. 12:368–370.

    Google Scholar 

  • Obrycki, J., K. L. Giles, and A. M. Ormond. 1998. Interactions between and introduced and indigenous coccinellid species at different prey densities. Oecologia 117: 279–285.

    Article  Google Scholar 

  • Parkman, J. P., J. H. Frank, K. B. Nguyen, and G. C. Smart. 1993a. Dispersal of Steinernema scapterisci (Rhabditida: Steinernematidae) after inoculative applications for mole cricket (Orthoptera: Gryllotalpidae) control in pastures. Biol. Control 3: 226–232.

    Article  Google Scholar 

  • Parkman, J. P., W. G. Hudson, J. H. Frank, K. B. Nguyen, and G. C. Smart. 1993b. Establishment and persistence of Steinernema scapterisci (Rhabditida: Steinernematidae) in field populations of Scapteriscus sp. mole crickets (Orthoptera: Gryllotalpidae). J. Entomol. Sci. 28:182–190.

    Google Scholar 

  • Pedigo, L. P., and L. G. Higley. 1992. The economic injury level concept and environmental quality: a new prospective. Am. Entomol. 38:12–21.

    Google Scholar 

  • Peters, A. 1996. The natural host range of Steinernema and Heterorhabditis sp., and their impact on insect populations. Biocontrol Sci., and Tech. 6:389–402.

    Article  Google Scholar 

  • Pimentel, D., C. Glenister, S. Fast, and D. Gallahan. 1984. Environmental risks of biological pest controls. Oikos 42: 283–290.

    Article  Google Scholar 

  • Pimentel, D., H. Acquay, M. Biltonen. p. Rice, M. Silva, J. Nelson, V. Lipner, S. Giordano, A. Horowitz, and M. D’Amore. 1992. Environmental and economic costs of pesticide use. Bioscience 42: 750–760.

    Article  Google Scholar 

  • Poinar, G. O., Jr. 1979. Nematodes for biological control of insects. CRC Press, Boca Raton, Florida. 277 p.

    Google Scholar 

  • Poinar, G. O. Jr. 1989. Non-insect hosts for the entomogenous rhabditoid nematodes Neoaplectana (Steinernematidae) and Heterorhabditis (Heterorhabditidae). Rev. Nematol. 12:423–428.

    Google Scholar 

  • Poinar, G. O., Jr. 1990. Biology and taxonomy of Steinernematidae and Heterorhabditidae. In R. Gaugler and H. K. Kaya (eds.), Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida. p. 23–62.

    Google Scholar 

  • Poinar, G. O. Jr., and A. Horn. 1986. Survival and horizontal movement of infective stage Neoaplectana carpocapsae in the field. J. Nematol. 18: 34–36.

    PubMed  CAS  Google Scholar 

  • Poinar, G. O., Jr., and G. M. Thomas. 1985a. Laboratory infection of spiders and harvestmen (Arachnida: Araneae and Opiliones) with Neoaplectana and Heterorhabditis nematodes (Rhabditoidea). J. Arachnol. 13:297–300.

    Google Scholar 

  • Poinar, G. O., Jr., and G. M. Thomas. 1985b. Laboratory infection of Garypus californicus (Pseudoscorpionida, Garypidae) with Neoaplectana and Heterorhabditis nematodes (Rhabditoidea). J. Arachnol. 13: 400–403.

    Google Scholar 

  • Poinar, G. O., Jr., and G. M. Thomas. 1988. Infection of frog tadpoles (Amphibia) by insect parasitic nematodes (Rhabditida). Experientia 44: 528–531.

    Article  Google Scholar 

  • Poinar, G. O., Jr., G. M. Thomas, S. B. Presser, and J. L. Hardy. 1982. Inoculation of entomogenous nematodes, Neoaplectana and Heterorhabditis, and their associated bacteria, Xenorhabdus sp., into chicks and mice. Environ. Entomol. 12:368–370.

    Google Scholar 

  • Proctor, D. L. C. 1984. Towards a biogeography of free-living soil nematodes. I. changing species richness, diversity and densities with changing latitudes. J. Biogeography 11: 103–117.

    Article  Google Scholar 

  • Raulston, J. R., S. D. Pair, J. Loera, and H. E. Cabanillas. 1992. Prepupal and pupal parasitism of Helicoverpa zea and Spodoptera frugiperda (Lepidoptera: Noctuidae) by Steinernema sp. in cornfields in the lower Rio Grande valley. J. Econ Entomol. 85: 1666–1670.

    Google Scholar 

  • Rosenheim, J. A., H. K. Kaya, L. E. Ehler, J. J. Marois, and B. A. Jaffee. 1995. Intraguild predation among biological control agents: theory and evidence. Biol. Control 5: 303–335.

    Article  Google Scholar 

  • Schroeder, W. J., and Beavers. 1987. Movement of entomogenous nematodes of the families Steinernematidae and Heterorhabditidae in soil. J. Nematol. 19: 257–259.

    PubMed  CAS  Google Scholar 

  • Schroeder, P. C., M. G. Villani, C. S. Ferguson, J. P. Nyrop, and E. J. Shields. 1993. Behavioral interactions between Japanese beetle (Coleoptera: Scarabaeidae) grubs and an entomopathogenic nematode (Nematoda: Heterorhabditidae) within turf microcosms. Environ. Entomol. 22: 595–600.

    Google Scholar 

  • Selvan, S., J. F. Campbell, and R. Gaugler. 1993. Density-dependent effects on entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) within an insect host. J. Invertebr. Pathol. 62:278–284.

    Article  Google Scholar 

  • Sexton, S. B., and P. Williams. 1981. A natural occurrence of parasitism of Graphognaththus leucoloma (Boheman) by the nematode Heterorhabditis sp. J. Austral. Entomol. Soc. 20:253–255.

    Article  Google Scholar 

  • Shanks, C. H., Jr., and F. Agudelo-Silva. 1990. Field pathogenicity and persistence of heterorhabditid and steinernematid nematodes (Nematoda) infecting black vine weevil larvae (Coleoptera: Curculionidae) in cranberry bogs. J. Econ. Entomol. 83: 107–110.

    Google Scholar 

  • Shapiro, D. I., and I. Glazer. 1996. Comparison of entomopathogenic nematode dispersal from infected hosts versus aqueous suspension. Environ. Entomol. 25: 1455–1461.

    Google Scholar 

  • Simberloff, D. 1992. Conservation of pristine habitats and unintended effects of biological control. In W. C. Kauffrnan and J. E. Nechols (eds.), Selection criteria and ecological consequances of importing natural enemies. Proc. Thomas Say Publ. Entomol., Entomological Soc. Amer., Lanham, Maryland. p. 101–117.

    Google Scholar 

  • Simberloff, D., and P. Stiling. 1996. How risky is biological control? Ecology 77: 1965–1974.

    Article  Google Scholar 

  • Simberloff, D., and P. Stiling. 1998. How risky is biological control?; reply. Ecology 79:1834–1836.

    Article  Google Scholar 

  • Simões, N., and J. S. Rosa. 1996. Pathogenicity and host specificity of entomopathogenic nematodes. Biocontrol Sci. Tech. 6:403–411.

    Article  Google Scholar 

  • Sloderbeck, P. E., and K. V. Yeargan. 1983. Green cloverworm populations in conventional and double-cropped no-till soybeans. J. Econ. Entomol. 76: 785–791.

    Google Scholar 

  • Small, R. W. 1987. A review of the prey of predatory soil nematodes. Pedobiologia 30: 179–206.

    Google Scholar 

  • Smits, P. H. 1996. Post-application persistence of entomopathogenic nematodes. Biocontrol Sci. Tech. 6:379–387.

    Article  Google Scholar 

  • Spiridonov, S. E., and D. A. Voronov. 1995. Small scale distribution of Steinernema feltiae juveniles in cultivated soil. In C. T. Griffin, R. L. Gwynn and J. P. Masson (eds.), Ecology and transmission strategies of entomopathogenic nematodes, European Commission, Luxembourg. p. 36–41.

    Google Scholar 

  • Stimac, J. L. 1990. Crop management systems and their effects on biological control of insects. In R. R. Baker and P. E. Dunn (eds.), New directions in biological control: Alternatives for suppressing agricultural pests and diseases. A. R. Liss, Inc. New York. p. 449–465.

    Google Scholar 

  • Stimac, J. L., and R. J. O’Neil. 1985. Integrating influences of natural enemies into models of crop/pest systems. In M. A. Hoy and D. C. Herzog. (eds.), Biological control in agricultural IPM systems. Academic Press, New York. p. 323–344.

    Google Scholar 

  • Stirling, G. R. 1991. Biological control of plant parasitic nematodes. CAB International, Wallingford, UK. 282 p.

    Google Scholar 

  • Strong, D. R., J. L. Maron, P. G. Connors, A. Whipple, S. Harrison and R. L. Jeffries. 1995. High mortality, fluctuation in numbers, and heavy subterranean insect herbivory in bush lupine, Lupinus arboreus. Oecologia 104: 85–92.

    Article  Google Scholar 

  • Strong, D. R., H. K. Kaya, A. V. Whipple, A. L. Child, S. Kraig, M. Bondonno, K. Dyer, and J. L. Maron. 1996a. Entomopathogenic nematodes: natural enemies of root-feeding caterpillars on bush lupine. Oecologia 108:167–173.

    Article  Google Scholar 

  • Strong, D. R., J. L. Maron, and P. G. Connors. 1996b. Top down from the underground: The underappreciated influence of subterranean food webs on above-ground ecology. In G. A. Polis, K. O. Winemiller (eds.), Food webs: integration of patterns and dynamics. Chapman and Hall, New York. p. 170–175.

    Google Scholar 

  • Stuart, R. J., and R. Gaugler. 1994. Patchiness in populations of entomopathogenic nematodes. J. Invertebr. Pathol. 64:39–45.

    Article  Google Scholar 

  • Timper. p., and H. K. Kaya. 1992. Impact of a nematode-parasitic fungus on the effectiveness of entomogenous nematodes. J. Nematol. 24: 1–8.

    PubMed  CAS  Google Scholar 

  • Timper, P., H. K. Kaya, and R. Gaugler. 1988. Dispersal of the entomogenous nematode Steinernema feltiae (Rhabditida: Steinernematidae) by infected adult insects. Environ. Entomol. 17: 546–50.

    Google Scholar 

  • Timper, P., H. K. Kaya, and B. A. Jaffee. 1991. Survival of entomogenous nematodes in soil infested with the nematode-parasitic fungus Hirsutella rhossiliensis (Deuteromycotina: Hyphomycetes). Biol. Control 1:42–50.

    Article  Google Scholar 

  • United Nations. 1992. Convention on Biological Diversity. Environmental Law and Institutions Programme Activity Center, United Nations Environment Program, New York.

    Google Scholar 

  • Van Der Werf, W., P. H. Smits, M. Downes, and C. Griffin. 1995. Concepts and prospects for modelling the efficacy and ecology of entomopathogenic nematodes. In C. T. Griffin, R. L. Gwynn and J. P. Masson (eds.), Ecology and transmission strategies of entomopathogenic nematodes. European Commission, Luxembourg. p. 42–51.

    Google Scholar 

  • Vänninen, I., G.-B. Husberg and H. M. T. Hokkanen. 1989. Occurrence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland. Acta Entomol. Fenn. 55: 65–71.

    Google Scholar 

  • Waage, J., and D. Greathead. 1988. Biological control: challenges and opportunities. Phil. Trans. Roy. So Lond. B 318: 111–128.

    Article  Google Scholar 

  • Walter, D. E. 1987a. Trophic behavior of ‘mycophagous’ microarthropods. Ecology 68: 226–229.

    Article  Google Scholar 

  • Walter, D. E. 1987b. Life history, trophic behaviour and description of_Gamasellodes vermivorax n. sp. (Mesostigmatoa: Ascidae), a predator of nematodes and arthropods in semiarid grassland soils. Can. J. Zool. 65: 1689–1695.

    Article  Google Scholar 

  • Walter, D. E. 1988a. Predation and mycophagy by endeostigmatid mites (Acariformes: Prostigmata). Exp. Appl.Acarol. 4:159–166.

    Article  Google Scholar 

  • Walter, D. E. 1988b. Nematophagy by soil arthropods from the shortgrass steppe, Chihauahuan Desert and Rocky Mountains of the central United States. Agric. Ecosyst. Environ. 24: 307–316.

    Article  Google Scholar 

  • Walter, D. E., and E. K. Ikonen. 1989. Species, guilds, and functional groups: taxonomy and behavior in nematophagous arthropods. J. Nematol. 21:315–327.

    PubMed  CAS  Google Scholar 

  • Walter, D. E., and D. T. Kaplan. 1990. Feeding observations on two astigmatic mites, Schwiebea rocketti (Acaridae) and Histiostoma bakeri (Histiostomatidae) associated with citrus feeder roots. Pedobiologia 34: 281–286.

    Google Scholar 

  • Walter, D. E., R. A. Hudgens, and D. W. Freckman. 1986. Consumption of nematodes by rungivorous mites, Tyrophagus sp. (Acarina: Astigmata: Acaridae). Oecologia 70: 357–361.

    Article  Google Scholar 

  • Walter, D. E., H. W. Hunt, and E. T. Elliot. 1987. The influence of prey type on the development and reproduction of some predatory soil mites. Pedobiologia 30: 419–424.

    Google Scholar 

  • Wasilewska, L. 1979. The structure and function of soil nematode communities in natural ecosystems and agrocenoses. Polish Ecological Studies 5: 97–145.

    Google Scholar 

  • Westerman, P. R. 1995. Comparative vertical migration of twenty one isolates of the insect parasitic nematode Heterorhabditis sp. in sand at 20°C. Fund. Appl. Nematol. 18: 149–158.

    Google Scholar 

  • Wilson, E. O. 1985. The biological diversity crisis: a challenge to science. Issues Sci. Tech. 2: 20–29.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer Science+Business Media New York

About this chapter

Cite this chapter

Barbercheck, M.E., Millar, L.C. (2000). Environmental Impacts of Entomopathogenic Nematodes Used for Biological Control in Soil. In: Follett, P.A., Duan, J.J. (eds) Nontarget Effects of Biological Control. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4577-4_17

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4577-4_17

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7067-3

  • Online ISBN: 978-1-4615-4577-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics