Influence of plants used in agricultural diversification on the nematode Heterorhabditis amazonensis
DOI:
https://doi.org/10.5433/1679-0359.2021v42n6SUPL2p3553Keywords:
Conservative biological control, Conservation, Entomopathogenic nematodes inundative control, Persistence.Abstract
In an agricultural system, to increase natural biological control, plants that attract natural enemies can be grown alongside the main crop. However, the effects of these plants on entomopathogenic nematodes (EPNs), important agents for controlling soil pests, and the action of their conservation are unknown. To assess the impact of these plants on EPNs, two experiments were carried out in a greenhouse. The first measured the effect of Crotalaria spectabilis, Crotalaria breviflora, and Tagetes erecta on the persistence and infectivity of Heterorhabditis amazonensis isolate RSC 5 for 27 days, compared to a control treatment without plants. The second trial evaluated the effect of C. breviflora and T. erecta on the displacement of the nematode. Additionally, the influence of predator Calosoma granulatum in this system was evaluated. The plants did not influence nematode behaviour in terms of persistence, infectivity, or displacement. However, C. spectabilis allowed the most significant persistence of nematodes in the substrate for a short time, and T. erecta caused the fastest suppression of the initial population of infectives juvenile. In the second experiment, neither the predator nor the plants affected the nematode's ability to move in the soil within 5 days. These results show that prior knowledge in agricultural diversification can help to control pests by inundative application of EPNs.Downloads
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References
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Araj, S., Shields, M. W., & Wratten, S. D. (2019). Weed floral resources and commonly used insectary plants to increase the efficacy of a whitefly parasitoid. BioControl, 64(5), 553-561. doi: 10.1007/s1052 6-019-09957-x
Baermann, G. (1917). Eine einfache methode zur auffindung von Ancylostomum (Nematoden) larven in erdproben. Geneeskunding Tijdschrift voor Nederlandsch-Indië, 57, 131-137.
Berriel, V., Monza, J., & Perdomo, C. H. (2020). Cover crop selection by jointly optimizing biomass productivity, biological nitrogen fixation, and transpiration efficiency: application to two Crotalaria species. Agronomy, 10(8), 1116. doi: 10.3390/agronomy10081116
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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(4), 417-422.
Ennis, D. E., Dillon, A. B., & Griffin, C. T. (2010). Simulated roots and host feeding enhance infection of subterranean insect by the entomopathogenic nematode Steinernema carpocapsae. Journal of Invertebrate Pathology, 103(2), 140-143. doi: 10.1016/j.jip.2009.11.004
Galbieri, R., Fuzattoii, M. G., Ciaii, E., Welteri, A. M., & Fanan, S. (2011). Desempenho de genótipos de algodoeiro na presença ou não de rotação de cultura com Crotalaria spectabilis, em área infestada com Meloidogyne incognita. Tropical Plant Pathology, 36(5), 303-307. doi: 10.1590/S1982-567620110005 00005
Gardiano, C. G., Dallemole-Giaretta, R., Lopes, E. A., Zooca, R. J. F., Ferraz, S., & Freitas, L. G. (2010). Atividade nematicide de extratos de sementes de espécies de Crotalaria sobre Meloidogyne javanica. Revista Trópica - Ciências Agrárias e Biológicas, 4(1), 1-5. doi: 10.0000/rtcab.v4i1.76
Gassmann, A. J., Stock, P., Tabashnik, B. E., & Singer, M. S. (2010). Tritrophic effects of host plants on a herbivore-pathogen interaction. Annals of the Entomological Society of America, 103(3), 371-378. doi: 10.1603/AN09130
Grubisic, D., Uroic, G., Ivosevic, A., & Grdisa, M. (2018). Nematode control by the use of antagonistic plants. Agriculturae Conspectus Scientificus, 83(4), 269-275. Retrieved from https://acs.agr.hr/acs/ index.php/acs/article/view/1518
Hass, B., Griffin, C. T., & Downes, M. J. (1999). Persistence of Heterorhabditis infective juveniles in soil: comparison of extraction and infectivity measurements. Journal of Nematologists, 31(4), 508-516. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2620384/
Hazir, S., Shapiro-Ilan, D. I., Hazir, C., Leite, L. G., Cakmak, I., & Olson, D. (2016). Multifaceted effects of host plants on entomopathogenic nematodes. Journal of Invertebrate Pathology, 135, 53-59. doi: 10.10 16/j.jip.2016.02.004
Helmberger, M. S., Shields, E. J., & Wickings, K. G. (2017). Ecology of belowground biological control: Entomopathogenic nematode interactions with soil biota. Applied Soil Ecology, 121, 201-213. doi: 10. 1016/j.apsoil.2017.10.013
Hodson, A. K., Siegel, J. P., & Lewis, E. E. (2012). Ecological influence of the entomopathogenic nematode, Steinernema carpocapsae, on pistachio orchard soil arthropods. Pedobiologia, 55(1), 51-58. doi: 10.10 16/j.pedobi.2011.10.005
Hooks, C. R. R., Wang, K. H., Ploeg, A., & McSorley, R. (2010). Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes. Applied Soil Ecology: A Section of Agriculture, Ecosystems & Environment, 46(3), 307-320. doi: 10.1016/j.apsoil.2010.09.005
Jagodic, A., Ipavec, N., Trdan, S., & Laznik, Z. (2017). Attraction behaviors: Are synthetic volatiles, typically emitted by insect-damaged Brassica nigra roots, navigation signals for entomopathogenic nematodes (Steinernema and Heterorhabditis)? Biocontrol, 62(4), 515-524. doi: 10.1007/s10526-017-9 796-x
Kanagy, J. M. N., & Kaya, H. K. (1996). The possible role of marigold roots and α-terthienyl in mediating host-finding by Steinernematid nematodes. Nematologica, 42(2), 220-231. doi: 10.1163/004325996X0 0066
Koppenhofer, A. M., Shapiro-Ilan, D. I., & Hitpold, I. (2020). Entomopathogenic nematodes in sustainable food production. Frontiers in Sustainable Food Systems, 4, 1-14. doi: 10.3389/fsufs.2020.00125
Lewis, E. E., & Clarke, D. J. (2012). Nematode parasites and entomopathogens. In F.Vega, & H. Kaya (Eds.), Insect pathology (pp. 395-424). Cambrige: Academic Press.
Mahmoud, M. F. (2016). Biology and use of entomopathogenic nematodes in insect pests biocontrol, a generic view. Cercetari Agronomice in Moldava, 49(4), 85-105. doi: 10.1515/cerce-2016-0039
Mertz, N. R., Agudelo, E. J. G., Sales, F. S., Rohde, C., & Moino, A., Jr. (2014). Phoretic dispersal of the entomopathogenic nematode Heterorhabditis amazonensis by the beetle Calosoma granulatum. Phytoparasitica, 42(2), 179-187. doi: 10.1007/s12600-013-0349-2
Osei, K., Gowen, S. R., Pembroke, B., Brandenburg, R. L., & Jordan, D. L. (2010). Potential of leguminous cover crops in management of a mixed population of root-knot nematodes (Meloidogyne spp.). Journal of Nematology, 42(3), 173-178. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC33804 90/
Parra, J. R. P. (1998). Raising insects for studies of pathogens. In S. B. Alves (Eds.), Microbial control of insects (pp. 1015-1037). Piracicaba: FEALQ.
Pasini, A. (1995). Biologia e técnica de criação do predador Calosoma granulatum Perty, 1830 (Coleoptera: Carabidae) em Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae), lagarta-da-soja. Tese de doutorado, Escola Superior de Agricultura “Luiz de Queiróz”, Piracicaba, SP, Brasil.
Poinar, G. O., Jr., & Grewal, P. S. (2012). History of entomopathogenic nematology. Journal of Nematology, 44(2), 153-161. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3578475/
Quispe, R., Mazón, M., & Rodríguez-Berrío, A. (2017). Do refuge plants favour natural pest control in maize crops? Insects, 8(3), 71. doi: 10.3390/insects8030071
Ratnadass, A., Fernandes, P., Avelino, J., & Habib, R. (2012). Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: a review. Agronomy for Sustainable Development, 32(1), 273-303. doi: 10.1007/s13593-011-0022-4
Santana, S. M., Dias-Arieira, C. R., Biela, F., Cunha, T. P. L., Chiamolera, F. M., Puerari, H. H., & Fontana, L. F. (2012). Manejo de Pratylenchus zeae por plantas antagonistas, em solos de áreas de cultivo de cana-de-açúcar. Nematropica, 42(1), 63-71. Retrieved from https://journals.flvc.org/nematropica/ article /view/79583
Santhi, V. S., Salame, L., Muklada, H., Azaizeh, H., Haj-Zaroubi, M., Awwad, S., Landau, S. Y., Glazer, I. (2019). Toxicity of phenolic compounds to entomopathogenic nematodes: a case study with Heterorhabditis bacteriophora exposed to lentisk (Pistacia lentiscus) extracts and their chemical components. Journal of Invertebrate Pathology, 160, 43-53. doi: 10.1016/j.jip.2018.12.003
Stuart, R. J., Barbercheck, M. E., & Grewal, P. S. (2015). Entomopathogenic nematodes in the soil environment: distribution interactions and the influence of biotic and abiotic factors. In: R. Campos-Herrera (Ed.), Nematode pathogenesis of insects as other pests (pp. 97-137). Dordrecht: Springer.
Supriyadi, R., Wijayanti, R., Arniputri, B., Puspitarini, N., & Dwiyatno, M. H. (2019). The effect of Crotalaria juncea plant in coffee ecosystem to the diversity and abundance of predators and parasitoids insects. IOP Conference Series: Earth and Environmental Science, 250(1), 1-6. doi: 10.1088/1755-13 15/250/1/012018
Tavares, W. S., Cruz, W. S. I., Silva, R. B., Figueiredo, M. L. C., Ramalho, F. S., Serrão, J. E. V., & Zanuncio, J. C. (2010). Soil organisms associated to the weed suppressant Crotalaria juncea (Fabaceae) and its importance as a refuge for natural enemies. Planta Daninha, 29(3), 473-479. doi: 10.1590/S010 0-83582011000300001
Thoden, T. C., & Boppré, M. (2010). Plants producing pyrrolizidine alkaloids: Sustainable too nematode management? Nematology, 12(1), 1-24. doi: 10.1163/138855409X12549869072248
Turlings, T. C. J., Hiltpold, I., & Rasmann, S. (2012). The importance of root-produces volatiles as foraging cues for entomopathogenic nematodes. Plant Soil, 358(1), 51-60. doi: 10.1007/s11104-012-1295-3
Woodring, J. L., & Kaya, H. K. (1988). Steinernematid and heterorhabditid nematodes: handbook of biology and techniques. Fayetteville: Arkansas Agricultural Experimental Station.
Andaló, V., Santos, V., Moreira, G. F., Moreira, C., Freire, M., & Moino, A. (2012). Movement of Heterorhabditis amazonensis and Steinernema arenarium in search of corn fall armyworm larvae in artificial conditions. Scientia Agricola, 69(3), 226-230. doi: 10.1590/S0103-90162012000300008
Araj, S., Shields, M. W., & Wratten, S. D. (2019). Weed floral resources and commonly used insectary plants to increase the efficacy of a whitefly parasitoid. BioControl, 64(5), 553-561. doi: 10.1007/s1052 6-019-09957-x
Baermann, G. (1917). Eine einfache methode zur auffindung von Ancylostomum (Nematoden) larven in erdproben. Geneeskunding Tijdschrift voor Nederlandsch-Indië, 57, 131-137.
Berriel, V., Monza, J., & Perdomo, C. H. (2020). Cover crop selection by jointly optimizing biomass productivity, biological nitrogen fixation, and transpiration efficiency: application to two Crotalaria species. Agronomy, 10(8), 1116. doi: 10.3390/agronomy10081116
Calabuche-Gómez, G., Regalado, R. E., Perera, D. G., Cabrera, I. M., Soler, D. M., & Hernández, M. G. R. (2019). Efecto de factores abióticos sobre la viabilidad e infectividade de Heterorhabditis amazonensis Andaló et al. cepa HC1. Revista de Protección Vegetal, 34(3), 1-9. Retrieved form http://scielo.sld.cu/ scielo.php?script=sci_arttext&pid=S1010-27522019000300004&lng=es&nrm=iso
Campos-Herrera, R., El-Borai, F. E., Martín, J. A. R., & Duncan, L. W. (2016). Entomopathogenic nematode food web assemblages in Florida natural areas. Soil Biology and Biochemistry, 93, 105-114. doi: 10.101 6/j.soilbio.2015.10.022
Campos-Herrera, R., Stuart, R. J., El-Borai, F., Gutierrez, C., & Duncan, L. (2010). Entomopathogenic nematode ecology and biological control in Florida citrus orchards. In A. Ciancio, & K. G. Mukerji (Eds.), Integrated management of arthropod pests and insect borne diseases (pp. 101-130). Dordrecht: Springer.
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(4), 417-422.
Ennis, D. E., Dillon, A. B., & Griffin, C. T. (2010). Simulated roots and host feeding enhance infection of subterranean insect by the entomopathogenic nematode Steinernema carpocapsae. Journal of Invertebrate Pathology, 103(2), 140-143. doi: 10.1016/j.jip.2009.11.004
Galbieri, R., Fuzattoii, M. G., Ciaii, E., Welteri, A. M., & Fanan, S. (2011). Desempenho de genótipos de algodoeiro na presença ou não de rotação de cultura com Crotalaria spectabilis, em área infestada com Meloidogyne incognita. Tropical Plant Pathology, 36(5), 303-307. doi: 10.1590/S1982-567620110005 00005
Gardiano, C. G., Dallemole-Giaretta, R., Lopes, E. A., Zooca, R. J. F., Ferraz, S., & Freitas, L. G. (2010). Atividade nematicide de extratos de sementes de espécies de Crotalaria sobre Meloidogyne javanica. Revista Trópica - Ciências Agrárias e Biológicas, 4(1), 1-5. doi: 10.0000/rtcab.v4i1.76
Gassmann, A. J., Stock, P., Tabashnik, B. E., & Singer, M. S. (2010). Tritrophic effects of host plants on a herbivore-pathogen interaction. Annals of the Entomological Society of America, 103(3), 371-378. doi: 10.1603/AN09130
Grubisic, D., Uroic, G., Ivosevic, A., & Grdisa, M. (2018). Nematode control by the use of antagonistic plants. Agriculturae Conspectus Scientificus, 83(4), 269-275. Retrieved from https://acs.agr.hr/acs/ index.php/acs/article/view/1518
Hass, B., Griffin, C. T., & Downes, M. J. (1999). Persistence of Heterorhabditis infective juveniles in soil: comparison of extraction and infectivity measurements. Journal of Nematologists, 31(4), 508-516. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2620384/
Hazir, S., Shapiro-Ilan, D. I., Hazir, C., Leite, L. G., Cakmak, I., & Olson, D. (2016). Multifaceted effects of host plants on entomopathogenic nematodes. Journal of Invertebrate Pathology, 135, 53-59. doi: 10.10 16/j.jip.2016.02.004
Helmberger, M. S., Shields, E. J., & Wickings, K. G. (2017). Ecology of belowground biological control: Entomopathogenic nematode interactions with soil biota. Applied Soil Ecology, 121, 201-213. doi: 10. 1016/j.apsoil.2017.10.013
Hodson, A. K., Siegel, J. P., & Lewis, E. E. (2012). Ecological influence of the entomopathogenic nematode, Steinernema carpocapsae, on pistachio orchard soil arthropods. Pedobiologia, 55(1), 51-58. doi: 10.10 16/j.pedobi.2011.10.005
Hooks, C. R. R., Wang, K. H., Ploeg, A., & McSorley, R. (2010). Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes. Applied Soil Ecology: A Section of Agriculture, Ecosystems & Environment, 46(3), 307-320. doi: 10.1016/j.apsoil.2010.09.005
Jagodic, A., Ipavec, N., Trdan, S., & Laznik, Z. (2017). Attraction behaviors: Are synthetic volatiles, typically emitted by insect-damaged Brassica nigra roots, navigation signals for entomopathogenic nematodes (Steinernema and Heterorhabditis)? Biocontrol, 62(4), 515-524. doi: 10.1007/s10526-017-9 796-x
Kanagy, J. M. N., & Kaya, H. K. (1996). The possible role of marigold roots and α-terthienyl in mediating host-finding by Steinernematid nematodes. Nematologica, 42(2), 220-231. doi: 10.1163/004325996X0 0066
Koppenhofer, A. M., Shapiro-Ilan, D. I., & Hitpold, I. (2020). Entomopathogenic nematodes in sustainable food production. Frontiers in Sustainable Food Systems, 4, 1-14. doi: 10.3389/fsufs.2020.00125
Lewis, E. E., & Clarke, D. J. (2012). Nematode parasites and entomopathogens. In F.Vega, & H. Kaya (Eds.), Insect pathology (pp. 395-424). Cambrige: Academic Press.
Mahmoud, M. F. (2016). Biology and use of entomopathogenic nematodes in insect pests biocontrol, a generic view. Cercetari Agronomice in Moldava, 49(4), 85-105. doi: 10.1515/cerce-2016-0039
Mertz, N. R., Agudelo, E. J. G., Sales, F. S., Rohde, C., & Moino, A., Jr. (2014). Phoretic dispersal of the entomopathogenic nematode Heterorhabditis amazonensis by the beetle Calosoma granulatum. Phytoparasitica, 42(2), 179-187. doi: 10.1007/s12600-013-0349-2
Osei, K., Gowen, S. R., Pembroke, B., Brandenburg, R. L., & Jordan, D. L. (2010). Potential of leguminous cover crops in management of a mixed population of root-knot nematodes (Meloidogyne spp.). Journal of Nematology, 42(3), 173-178. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC33804 90/
Parra, J. R. P. (1998). Raising insects for studies of pathogens. In S. B. Alves (Eds.), Microbial control of insects (pp. 1015-1037). Piracicaba: FEALQ.
Pasini, A. (1995). Biologia e técnica de criação do predador Calosoma granulatum Perty, 1830 (Coleoptera: Carabidae) em Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae), lagarta-da-soja. Tese de doutorado, Escola Superior de Agricultura “Luiz de Queiróz”, Piracicaba, SP, Brasil.
Poinar, G. O., Jr., & Grewal, P. S. (2012). History of entomopathogenic nematology. Journal of Nematology, 44(2), 153-161. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3578475/
Quispe, R., Mazón, M., & Rodríguez-Berrío, A. (2017). Do refuge plants favour natural pest control in maize crops? Insects, 8(3), 71. doi: 10.3390/insects8030071
Ratnadass, A., Fernandes, P., Avelino, J., & Habib, R. (2012). Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: a review. Agronomy for Sustainable Development, 32(1), 273-303. doi: 10.1007/s13593-011-0022-4
Santana, S. M., Dias-Arieira, C. R., Biela, F., Cunha, T. P. L., Chiamolera, F. M., Puerari, H. H., & Fontana, L. F. (2012). Manejo de Pratylenchus zeae por plantas antagonistas, em solos de áreas de cultivo de cana-de-açúcar. Nematropica, 42(1), 63-71. Retrieved from https://journals.flvc.org/nematropica/ article /view/79583
Santhi, V. S., Salame, L., Muklada, H., Azaizeh, H., Haj-Zaroubi, M., Awwad, S., Landau, S. Y., Glazer, I. (2019). Toxicity of phenolic compounds to entomopathogenic nematodes: a case study with Heterorhabditis bacteriophora exposed to lentisk (Pistacia lentiscus) extracts and their chemical components. Journal of Invertebrate Pathology, 160, 43-53. doi: 10.1016/j.jip.2018.12.003
Stuart, R. J., Barbercheck, M. E., & Grewal, P. S. (2015). Entomopathogenic nematodes in the soil environment: distribution interactions and the influence of biotic and abiotic factors. In: R. Campos-Herrera (Ed.), Nematode pathogenesis of insects as other pests (pp. 97-137). Dordrecht: Springer.
Supriyadi, R., Wijayanti, R., Arniputri, B., Puspitarini, N., & Dwiyatno, M. H. (2019). The effect of Crotalaria juncea plant in coffee ecosystem to the diversity and abundance of predators and parasitoids insects. IOP Conference Series: Earth and Environmental Science, 250(1), 1-6. doi: 10.1088/1755-13 15/250/1/012018
Tavares, W. S., Cruz, W. S. I., Silva, R. B., Figueiredo, M. L. C., Ramalho, F. S., Serrão, J. E. V., & Zanuncio, J. C. (2010). Soil organisms associated to the weed suppressant Crotalaria juncea (Fabaceae) and its importance as a refuge for natural enemies. Planta Daninha, 29(3), 473-479. doi: 10.1590/S010 0-83582011000300001
Thoden, T. C., & Boppré, M. (2010). Plants producing pyrrolizidine alkaloids: Sustainable too nematode management? Nematology, 12(1), 1-24. doi: 10.1163/138855409X12549869072248
Turlings, T. C. J., Hiltpold, I., & Rasmann, S. (2012). The importance of root-produces volatiles as foraging cues for entomopathogenic nematodes. Plant Soil, 358(1), 51-60. doi: 10.1007/s11104-012-1295-3
Woodring, J. L., & Kaya, H. K. (1988). Steinernematid and heterorhabditid nematodes: handbook of biology and techniques. Fayetteville: Arkansas Agricultural Experimental Station.
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2021-10-08
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Mertz, N. R., Sales, F. S., Agudelo, E. J. G., & Moino Junior, A. (2021). Influence of plants used in agricultural diversification on the nematode Heterorhabditis amazonensis. Semina: Ciências Agrárias, 42(6SUPL2), 3553–3566. https://doi.org/10.5433/1679-0359.2021v42n6SUPL2p3553
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