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Phytoparasitica

, Volume 42, Issue 2, pp 179–187 | Cite as

Phoretic dispersal of the entomopathogenic nematode Heterorhabditis amazonensis by the beetle Calosoma granulatum

  • Natalia Ramos Mertz
  • Elsa Judith Guevara Agudelo
  • Fernanda Soares Sales
  • Cristhiane Rohde
  • Alcides Moino Jr.
Article

Abstract

Entomopathogenic nematodes (EPN) have limited ability to travel and need to adopt alternative strategies to reach hosts that are far away. They can attach themselves to an organism that acts only as a dispersal agent to transport the EPN to places that they cannot reach by themselves. The larval and adult stages of Calosoma granulatum (Coleoptera: Carabidae) beetle are important predators of caterpillars that live in the soil of Brazilian agricultural systems. The nematode Heterorhabditis amazonensis (Rhabditida: Heterorhabditidae) is a native of Brazil and plays a major role in the control of Spodoptera frugiperda (Lepidoptera: Noctuidae) caterpillars. This study assessed the ability of C. granulatum to carry and disperse H. amazonensis. The experimental arenas consisted of two types of containers with substrate connected by a plastic tube through which the insects could move freely. Only one of the containers received infective juveniles (IJ) and the other was used as the test container. We first used C. granulatum larvae and adults to evaluate the influence of different concentrations of IJs on phoretic behavior. Then different distances traveled by the adult beetle were tested to measure their effect on IJ transport. The results showed that C. granulatum is a good phoretic dispersal agent and the transport of IJs by the larvae is less influenced than transport by the adult, by a change in the IJ concentration. The distance traveled by the adult influences the number of EPN carried and the detection of phoresy even at greater distances (40 cm) indicates that C. granulatum is capable of transporting the EPN for distances greater than those evaluated.

Keywords

Biological control Entomopathogen Non-target organism Transportation 

References

  1. Allen, R. T. (1977). Calosoma (Castrida) alternans granulatum Perty: a predator of cotton leaf worms in Bolivia (Coleoptera: Carabidae: Carabini). The Coleopterists Bulletin, 31, 73–76.Google Scholar
  2. Andaló, V., Nguyen, K. N., & Moino-Jr, A. (2006). Heterorhabditis amazonensis n. sp. (Rhabditida: Heterorhabditidae) from Amazonas, Brasil. Nematology, 8, 853–867.CrossRefGoogle Scholar
  3. Andaló, V., Santos, V., Moreira, G. F., Moreira, C. C., Freire, M., & Moino-Jr, A. (2012). Movement of Heterorhabditis amazonensis and Steinernema arenarium in search of corn fall armyworm larvae in artificial conditions. Scientia Agricola, 69, 226–230.CrossRefGoogle Scholar
  4. Andaló, V., Santos, V., Moreira, G. F., Moreira, C. C., & Moino-Jr, A. (2010). Evaluation of entomopathogenic nematodes under laboratory and greenhouse conditions for the control of Spodoptera frugiperda. Ciência Rural, 40, 1860–1866.CrossRefGoogle Scholar
  5. Baermann, G. (1917). Eine einfache Methode zur Auffindung von Ancylostomum (Nematoden) Larven in Erdproben. Geneeskunding Tijdschrift voor Nederlandsch-Indië, 57, 131–137.Google Scholar
  6. Batista, E. S. de P., Auad, A. M., Resende, T. T., & Monteiro, C. M. O. (2011). Screening of entomopathogenic nematodes to control Mahanarva fimbriolata (Hemiptera: Cercopidae). Revista Colombiana de Entomologia, 37, 198-202Google Scholar
  7. Best, R. L., & Beegle, C. C. (1977). Consumption of Agrotis ipsilon by several species of Carabids found in Iowa. Environmental Entomology, 6, 532–534.Google Scholar
  8. Brust, G. E., Stinner, B. R., & McCartney, D. A. (1986). Predator activity and predation in corn agroecosystems. Environmental Entomology, 15, 1017–1021.Google Scholar
  9. Capinera, J. L., & Barbosa, P. (1975). Transmission of nuclear-polyhedrosis virus to gypsy moth larvae by Calosoma sycophanta. Annals of the Entomological Society of America, 68, 593–594.Google Scholar
  10. Chocorosqui, V. R., & Pasini, A. (2000). Predação de pupas de Alabama argillacea (Hubner) (Lepidoptera: Noctuidae) por larvas e adultos de Calosoma granulatum Perty (Coleoptera: Carabidae) em laboratório. Anais da Sociedade Entomológica Brasileira, 29, 65–70.CrossRefGoogle Scholar
  11. Choo, H. Y., & Kaya, H. K. (1991). Influence of soil texture and presence of roots on host finding by Heterorhabditis bacteriophora. Journal of Invertebrate Pathology, 58, 279–280.CrossRefGoogle Scholar
  12. Cividanes, F. J., Barbosa, J. C., Ide, S., Perioto, N. W., & Lara, R. I. R. (2009). Faunistic analysis of Carabidae and Staphylinidae (Coleoptera) in five agroecosystems in northeastern São Paulo state, Brazil. Pesquisa Agropecuária Brasileira, 44, 954–958.CrossRefGoogle Scholar
  13. Curran, J., & Heng, J. (1992). Comparison of three methods for estimating the number of entomopathogenic nematodes present in soil samples. Journal of Nematology, 24, 170–176.PubMedCentralPubMedGoogle Scholar
  14. Dillon, A. B., Downes, M. J., Ward, D., & Griffin, C. T. (2007). Optimizing application of entomopathogenic nematodes to manage large pine weevil, Hylobius abietis L. (Coleoptera: Curculionidae) populations developing in pine stumps, Pinus sylvestris. Biological Control, 40, 253–263.CrossRefGoogle Scholar
  15. Dutky, S. R., Thompson, J. V., & Cantwe, G. E. (1964). A technique for the mass propagation of the DD-136 nematode. Journal of Insect Pathology, 6, 417–422.Google Scholar
  16. Eng, M. S., Preisser, E. L., & Strong, D. R. (2005). Phoresy of the entomopathogenic nematode Heterorhabditis marelatus by a non-host organism, the isopod Porcellio scaber. Journal of Invertebrate Pathology, 88, 173–176.PubMedCrossRefGoogle Scholar
  17. Epsky, N. D., Walter, D. E., & Capinera, J. L. (1988). Potential role of nematophagous microarthropods as biotic mortality factors of entomogenous nematodes (Rhabditida: Steinernematidae, Heterorhabditidae). Journal of Economic Entomology, 81, 821–825.Google Scholar
  18. Ferraz, L. C. C. B. (1998). Nematóides entomopatogênicos, (pp. 541–569). In: S. B. A. Alves (Ed.) Controle microbiano de insetos. Piracicaba, Brazil: FEALQ.Google Scholar
  19. Georgis, R., Koppenhöfer, A. M., Lacey, L. A., Bélair, G., Duncan, L. W., Grewal, P. S., et al. (2006). Successes and failures in the use of parasitic nematodes for pest control. Biological Control, 38, 103–123.Google Scholar
  20. Georgis, R., & Poinar, G. O., Jr. (1983). Effect of soil texture on the distribution and infectivity of Neoplactana glaseri (Nematoda: Steinernematidae). Journal of Nematology, 15, 329–332.PubMedCentralPubMedGoogle Scholar
  21. Gidaspow, T. (1963). The genus Calosoma in Central America, the Antilles, and South America (Coleoptera: Carabidae). Bulletin of American Museum of Natural History, 124, 275–314.Google Scholar
  22. Gouge, D. H., Smith, K. A., Lee, L. L., & Henneberry, T. J. (2000). Effect of soil depth and moisture on the vertical distribution of Steinernema ribrave (Nematoda: Steinernematidae). Journal of Nematology, 32, 223–228.PubMedCentralPubMedGoogle Scholar
  23. Grewal, P. S., de Nardo, E. A. B., & Aguillera, M. M. (2001). Entomopathogenic nematodes: Potential for exploration and use in South America. Neotropical Entomology, 30, 191–205.CrossRefGoogle Scholar
  24. Gullan, P. J., & Cranston, P. S. (2005). Insect development and life histories, (pp. 142–176). In: P. J. Gullan & P. S. Cranston (Eds.) The insects: an outline of entomology. Oxford, UK: Blackwell Publishing Ltd.Google Scholar
  25. Kaya, H. K., & Gaugler, R. (1993). Entomopathogenic nematodes. Annual Review of Entomology, 38, 181–206.CrossRefGoogle Scholar
  26. Knell, R. J., & Webberley, K. M. (2004). Sexually transmitted diseases of insects: distribution, evolution, ecology and host behavior. Biological Reviews, 79, 557–581.PubMedCrossRefGoogle Scholar
  27. Kruitbos, L. M., Heritage, S., & Wilson, M. J. (2009). Phoretic dispersal of entomopathogenic nematodes by Hylobius abietis. Nematology, 11, 419–427.CrossRefGoogle Scholar
  28. Leite, L. G., Machado, L. A. M., Goulart, R. M., Tavares, F. M., & Batista Filho, A. (2005). Screening of entomopathogenic nematodes (Nemata: Rhabditida) and the efficiency of Heterorhabditis sp. against the sugarcane root spittlebug Mahanarva fimbriolata (Fabr.) (Hemiptera: Cercopidae). Neotropical Entomology, 34, 785–790.CrossRefGoogle Scholar
  29. Lim, U. T., & van Driesche, R. G. (2005). A new potential host and transmission routes of Thripinema nicklewoodi, an entomogenous nematode of western flower thrips. Biological Control, 33, 49–55.CrossRefGoogle Scholar
  30. Lovei, G. L., & Sunderland, K. D. (1996). Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41, 231–256.PubMedCrossRefGoogle Scholar
  31. Macmillan, K., Haukeland, S., Rae, R., Young, I., Crawford, J., Hapca, S., et al. (2009). Dispersal patterns and behavior of the nematode Phasmarhabditis hermaphrodita in mineral soils and organic media. Soil Biology & Biochemistry, 41, 1483–1490.CrossRefGoogle Scholar
  32. Malan, A. P., & Manrakhan, A. (2009). Susceptibility of the Mediterranean fruit fly (Ceratitis capitata) and the Natal fruit fly (Ceratitis rosa) to entomopathogenic nematodes. Journal of Invertebrate Pathology, 100, 47–49.PubMedCrossRefGoogle Scholar
  33. Monteiro, C. M. O., Prata, M. C. A., Furlong, J., Faza, A. P., Mendes, A. S., Andaló, V., et al. (2010). Heterorhabditis amazonensis (Rhabditidae: Heterorhabditidae) strain RSC-5, for biological control of the cattle tick Rhipicephalus (Boophilus) microplu (Acari: Ixodidae). Parasitology Research, 106, 821–826.PubMedCrossRefGoogle Scholar
  34. Parkman, J. P., Frank, J. H., Nguyen, K. B., & Smart, G. C., Jr. (1993). Dispersal of Steinernema scapterisci (Rhabditida: Steinernematidae) after inoculative applications for mole cricket (Orthoptera: Gryllotalpidae) control in pastures. Biological Control, 3, 226–232.CrossRefGoogle Scholar
  35. Parra, J. R. P. (1998). Raising insects for studies of pathogens, (pp. 1015–1037). In: S. B. Alves (Ed.) Microbial control of insects. Piracicaba, Brazil: FEALQ.Google Scholar
  36. Pasini, A., & Foerster, L. A. (1996). Ritmo diário de atividade e dispersão de Calosoma granulatum P. (Coleoptera: Carabidae) na cultura da soja. Anais da Sociedade Entomológica do Brasil, 25, 395–399.Google Scholar
  37. Pegoraro, R. A., & Foerster, L. A. (1985). Observações sobre o ciclo evolutivo e hábitos alimentares de Calosoma granulatum Perty, 1830 (Coleoptera: Carabidae) em laboratório. Anais da Sociedade Entomológica do Brasil, 14, 269–275.Google Scholar
  38. Pegoraro, R. A., & Foerster, L. A. (1988). Abundância e distribuição de larvas e adultos de Calosoma granulatum Perty, 1830 (Coleoptera: Carabidae) dentre cultivares de soja em diferentes épocas de semeadura. Anais da Sociedade Entomológica do Brasil, 17, 237–248.Google Scholar
  39. Poinar, G. O., Jr. (1972). Nematodes as facultative parasites of insects. Annual Review of Entomology, 17, 103–122.CrossRefGoogle Scholar
  40. Riddick, E. W., & Mills, N. J. (1994). Potential of adult carabids (Coleoptera: Carabidae) as predators of fifth-instar codling moth (Lepidoptera: Tortricidae) in apple orchards in California. Environmental Entomology, 23, 1338–1345.Google Scholar
  41. Robinson, A. F., & Heald, C. M. (1989). Accelerated movement of nematodes from soil in Baermann funnels with temperature gradients. Journal of Nematotology, 21, 370–378.Google Scholar
  42. Santos, V., Moino, A., Jr., Andaló, V., Moreira, C. C., & Olinda, R. A. (2011). Virulence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) for the control of Diabrotica speciosa Germar (Coleoptera: Chrysomelidae). Ciência e Agrotecnologia, 35, 1149–1156.CrossRefGoogle Scholar
  43. Shapiro, D. I., Berry, E. C., & Lewis, L. C. (1993). Interactions between nematodes and earthworms: enhanced dispersal of Steinernema carpocapsae. Journal of Nematology, 25, 189–192.PubMedCentralPubMedGoogle Scholar
  44. Shapiro, D. I., & Brown, I. (2013). Earthworms as phoretic hosts for Steinernema carpocapsae and Beauveria bassiana: Implications for enhanced biological control. Biological Control, 66, 41–48.CrossRefGoogle Scholar
  45. Shapiro, D. I., Tylka, G. L., Berry, E. C., & Lewis, L. C. (1995). Effects of earthworms on the dispersal of Steinernema spp. Journal of Nematology, 27, 21–28.PubMedCentralPubMedGoogle Scholar
  46. Stehr, F. W. (1991). Immature insects. Dubuque, IA, USA: Kendall/Hunt Publishing Company.Google Scholar
  47. Suenaga, H., & Hamamura, T. (1998). Laboratory evaluation of carabid beetles (Coleoptera: Carabidae) as predators of diamondback moth (Lepidoptera: Plutellidae) larvae. Biological Control, 27, 767–772.Google Scholar
  48. Toepfer, S., Hatala-Zseller, I., Ehlers, R. U., Peters, A., & Kuhlmann, U. (2010). The effect of application techniques on field-scale efficacy: can the use of entomopathogenic nematodes reduce damage by western corn rootworm larvae? Agricultural and Forest Entomology, 12, 389–402.CrossRefGoogle Scholar
  49. Wang, Y., & Gaugler, R. (1998). Host and penetration site location by entomopathogenic nematodes against Japanese beetle larvae. Journal of Invertebrate Pathology, 72, 313–318.PubMedCrossRefGoogle Scholar
  50. Wilson, M. J., Lewis, E. E., Yoder, F., & Gaugler, R. (2003). Application pattern and persistence of the entomopathogenic nematode Heterorhabditis bacteriophora. Biological Control, 26, 180–188.CrossRefGoogle Scholar
  51. Woodring, J. L., & Kaya, H. K. (1988). Steinernematid and Heterorhabditid nematodes: handbook of biology and techniques. Southern Cooperative Series Bulletin. Fayetteville, Arkansas Agricultural Experimental Station.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Natalia Ramos Mertz
    • 1
  • Elsa Judith Guevara Agudelo
    • 1
  • Fernanda Soares Sales
    • 1
  • Cristhiane Rohde
    • 2
  • Alcides Moino Jr.
    • 1
  1. 1.Insect Pathology Laboratory, Department of EntomologyUniversidade Federal de LavrasLavrasBrazil
  2. 2.Universidade Federal Fronteira SulLaranjeiras do SulBrazil

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