Abstract
The interaction between the mirid predator Engytatus varians (Distant) and a Mexican isolate (SeSIN6) of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) was examined under laboratory conditions. In a choice test, E. varians females and males demonstrated no preference for virus-infected Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) second instar compared with non-infected at two different post-inoculation times (48 and 72 h). Similarly, prey search time (5–6 h) did not differ significantly for each type of prey. Bioassays were performed to confirm the viability of occlusion bodies (OBs) from predator’s faces collected at 48, 96, and 144 h after exposure to virus-infected S. exigua larvae. The proportion of larval mortality was between 0.20 and 0.62 across all times and both E. varians sexes. Another experiment was performed to evaluate the dispersal of SeSIN6 OBs by physical contact with E. varians adults on tomato (Solanum lycopersicum Miller) leaflets treated with the pathogen. Engytatus varians adults were exposed to OB-treated tomato leaflets during 24 or 48 h using a clip cage. After each exposure time, these adults were removed and placed on clean uncontaminated leaflets for periods of 4–48 h. These leaflets were then exposed to groups of S. exigua second instars in clip cages. The proportion of virus-induced larval mortality of S. exigua (ranging from 0.45 to 1.0) was significantly affected by the duration of exposure of E. varians adults on OB-treated or untreated tomato leaflets. Our results reveal the potential of E. varians as an agent for the dispersal of SeMNPV OBs.
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References
Abbas MST, Boucias DG (1984) Interaction between nuclear polyhedrosis virus-infected Anticarsia gemmatalis (Lepidoptera: Noctuidae) larvae and predator Podisus maculiventris (Say) (Hemiptera: Pentatomidae). Environ Entomol 13(2):599–602. https://doi.org/10.1093/ee/13.2.599
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267. https://doi.org/10.1093/jee/18.2.265a
Biever KD, Andrews PL, Andrews PA (1982) Use of a predator, Podisus maculiventris, to distribute virus and initiate epizootics. J Econ Entomol 75(1):150–152. https://doi.org/10.1093/jee/75.1.150
Black J (2017) Horizontal transmission of Helicoverpa armigera NPV in soybean fields infested with Heliothis zea. Master of Science dissertation, University of Arkansas, US, p 105. http://scholarworks.vark.edu/etd/2533
Burla JP, Carpintero DL, Castiglioni E (2021) First report of Engytatus varians (Distant, 1884) (Heteroptera: Miridae: Dicyphini) in Eastern Uruguay and preliminary test on its feeding habits. Entomol Commun, pp ec03021–ec03021. https://doi.org/10.37486/2675-1305.ec03021
Cabodevilla O, Ibañez I, Simón O, Murillo R, Caballero P, Williams T (2011) Occlusion body pathogenicity, virulence and productivity traits vary with transmission strategy in a nucleopolyhedrovirus. Biol Control 56:184–192. https://doi.org/10.1016/j.biocontrol.2010.10.007
Castillejos V, García L, Cisneros J, Goulson D, Cave RD, Caballero P, Williams T (2001) The potential of Chrysoperla rufilabris and Doru taeniatum as agents for dispersal of Spodoptera frugiperda nucleopolyhedrovirus in maize. Entomol Experiment Et Applicata 98(3):353–359. https://doi.org/10.1046/j.1570-7458.2001.00792.x
Castineiras A (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in Cuba. Fla Entomol 78:538–540. https://doi.org/10.2307/3495540
Chambers AC, Aksular M, Graves LP, Irons SL, Possee RD, King LA (2018) Overview of the baculovirus expression system. Curr Protoc Protein Sci 91:541–546. https://doi.org/10.1002/cpps.47
Cory JS (2015) Insect virus transmission: different routes to persistence. Curr Opin Ins Sci 8:130–135. https://doi.org/10.1016/j.cois.2015.01.007
Cory JS, Hails RS, Sait SM (1997) Baculovirus ecology. In: Miller LK (ed) The baculoviruses. Plenum Press, New York, pp 301–339
Erlandson MA, Toprak U, Hegedus DD (2019) Role of the peritrophic matrix in insect-pathogen interactions. J Ins Physiol 117:103894. https://doi.org/10.1016/j.jinsphys.2019.103894
Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25(2):140–146. https://doi.org/10.1046/j.1365-2311.2000.00243.x
Ferreira PSF, Da Silva ER, Coelho LBN (2001) Miridae (Heteroptera) fitófagos e predadores de Minas Gerais, Brasil, com ênfase em espécies com potencial econômico. Iheringia Sér Zool 91:159–169. https://doi.org/10.1590/S0073-47212001000200022
Fialho MC, Moreira NR, Zanuncio JC, Ribeiro AF, Terra WR, Serrão JE (2012) Prey digestion in the midgut of the predatory bug Podisus nigrispinus (Hemiptera: Pentatomidae). J Insect Physiol 58(6):850–856. https://doi.org/10.1016/j.jinsphys.2012.03.009
Fuxa JR, Richter AR (2001) Quantification of soil-to-plant transport of recombinant nucleopolyhedrovirus: effects of soil type and moisture, air currents, and precipitation. Appl Environ Microbiol 67:5166–5170. https://doi.org/10.1128/AEM.67.11.5166-5170.2001
Hafeez M, Ullah F, Musa Khan M, Li X, Zhang Z, Shah S, Imran M, Assiri MA, Fernández-Grandon GM, Desneux N, Rehman M, Fahad S, Lu Y (2022) Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review. Environ Sci Pollut Res 29:1746–1762. https://doi.org/10.1007/s11356-021-16974-w
Hernández LM, Henry TJ (2010) The plant bugs, or Miridae (Hemiptera: Heteroptera), of Cuba. Pensoft Publishers, Sofia and Moscow
Hughes PR, Wood HA (1981) A synchronous peroral technique for the bioassay of insect viruses. J Invertebr Pathol 37(2):154–159. https://doi.org/10.1016/0022-2011(81)90069-0
Martínez AM, Baena M, Figueroa JI, Del Estal P, Medina M, Guzmán-Lara E, Pineda S (2014) Primer registro de Engytatus varians (Distant) (Hemiptera: Heteroptera: Miridae) en México y su depredación sobre Bactericera cockerelli (Šulc) (Hemiptera: Triozidae): una revisión de su distribución y hábitos. Acta Zool Mex (NS) 30(3):617–624. https://doi.org/10.21829/azm.2014.30381
Nicholls-Estrada CI (2008) Control biológico de insectos: un enfoque agroecológico, vol 2. Editorial Universidad de Antioquia, Medellín.
Pérez-Aguilar DA, Martínez AM, Viñuela E, Figueroa JI, Gómez-Ramos B, Morales SI, Tapia A, Pineda S (2019) Impact of the zoophytophagous predator Engytatus varians (Hemiptera: Miridae) on Bactericera cockerelli (Hemiptera: Triozidae) control. Biol Control 132:29–35. https://doi.org/10.1016/j.biocontrol.2018.12.009
Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A (2015) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88(3):543–554. https://doi.org/10.1007/s10340-014-0640-0
Pineda S, Hernández-Quintero O, Velázquez-Rodríguez YB, Viñuela E, Figueroa JI, Morales SI, Martínez-Castillo AM (2020) Predation by Engytatus varians (Distant) (Hemiptera: Miridae) on Bactericera cockerelli (Sulcer) (Hemiptera: Triozidae) and two Spodoptera species. Bull Entomol Res 110(2):270–277. https://doi.org/10.1017/S0007485319000579
Poitout S, Bues R (1974) Élevage de chenilles de vingthuit espéces de lépidoptéres Noctuidae et de deux espéces d’Arctiidae sur milieu artificiel simple. Particularités de l’élevage selon les espéces. Ann Zool Ecol Anim 6:431–441
Rabelo MM, Santos IB, Paula-Moraes SV (2022) Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae) fitness and resistance stability to diamide and pyrethroid insecticides in the United States. Insects 13(4):365. https://doi.org/10.3390/insects13040365
Saini E, Quintana G, Rios M (1997) Interacción entre el depredador Podisus connexivus (Heteroptera: Pentatomidae) y el virus de la poliedrosis nuclear de Rachiplusia nu (Lepidoptera: Noctuidae) en condiciones de laboratorio. Rev Soc Entomol Arg 56:105–108
Samir M, Abbas T (2020) Interactions between baculoviruses and entomophagous insects. Egypt J Biol Pest Control 30:107. https://doi.org/10.1186/s41938-020-00306-0
Steiner AA (1984) The universal nutrient solution. Proceedings 6th international congress on soilless culture. Wageningen, The Netherlands, pp 633–650
Sugiura S (2020) Predators as drivers of insect defenses. Entomol Sci 23(3):316–337. https://doi.org/10.1111/ens.12423
Thézé J, Lopez-Vaamonde C, Cory JS, Herniou EA (2018) Biodiversity, evolution and ecological specialization of baculoviruses: a treasure trove for future applied research. Viruses 10(7):366. https://doi.org/10.3390/v10070366
Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenuis (Het.: Miridae). Biocontrol Sci Tech 15:513–518. https://doi.org/10.1080/09583150500088777
Van Driesche R, Hoddle M, Center TD (2007) Control de plagas y malezas por enemigos naturales. U.S Department of Agriculture, Washington, D.C.
Vasconcelos SD, Williams T, Hails RS (1996) Prey selection and baculovirus dissemination by carabid predators of Lepidoptera. Ecol Entomol 21:98–104. https://doi.org/10.1111/j.1365-2311.1996.tb00271.x
Virto C, Navarro D, Tellez MM, Herrero S, Williams T, Murillo R, Caballero P (2014) Natural populations of Spodoptera exigua are infected by multiple viruses that are transmitted to their offspring. J Invertebr Pathol 122:22–27. https://doi.org/10.1016/j.jip.2014.07.007
Williams T (2018) Viruses. In: Hajek AE, Shapiro-Ilan DI (eds) Ecology of Invertebrate Diseases. Wiley, Chichester, pp 215–228. https://doi.org/10.1002/9781119256106.ch7
Williams T, Lopez-Ferber M, Caballero P (2021) Nucleopolyhedrovirus coocclusion technology: A new concept in the development of biological insecticides. Front Microbiol 12:810026. https://doi.org/10.3389/fmicb.2021.810026
Young SY, Kring TJ (1991) Selection of healthy and nuclear polyhedrosis virus infected Anticarsia gemmatalis (Lep.: Noctuidae) as prey by nymphal Nabis roseipennis (Hemiptera: Nabidae) in laboratory and on soybean. Entomophaga 36(2):265–273. https://doi.org/10.1007/BF02374562
Young SY, Yearian WC (1987) Nabis roseipennis adults (Hemiptera: Nabidae) as disseminators of Nuclear Polyhedrosis Virus to Anticarsia gemmatalis (Lepidoptera: Noctuidae) Larvae. Environ Entomol 16(6):1330–1333. https://doi.org/10.1093/ee/16.6.1330
Zamora-Avilés N, Murillo R, Lasa R, Pineda S, Figueroa JI, Bravo-Patinõ A, Martínez AM (2017) Genetic and biological characterization of four nucleopolyhedrovirus isolates collected in Mexico for the control of Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol 110(4):1465–1475. https://doi.org/10.1093/jee/tox130
Zheng XL, Cong XP, Wang XP, Lei CL (2011) A review of geographic distribution, overwintering and migration in Spodoptera exigua Hübner (Lepidoptera: Noctuidae). J Entomol Res 13(3):39–48
Zheng XL, Huang QC, Cao WZ, Lu W, Wang GQ, Yu SZ, Zhen-De Y, Wang XP (2015) Modeling climate change impacts on overwintering of Spodoptera exigua Hübner in regions of China. Chil J Agric Res 75(3):328–333. https://doi.org/10.4067/S0718-58392015000400009
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This work was supported by the Coordinación de la Investigación Científica, Universidad Michoacana de San Nicolás de Hidalgo.
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Martínez, A.M., Zamudio-López, S., Guzmán-Pedraza, A.O. et al. Engytatus varians as agent for dispersal of Spodoptera exigua nucleopolyhedrovirus. J Pest Sci 95, 1621–1630 (2022). https://doi.org/10.1007/s10340-022-01549-6
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DOI: https://doi.org/10.1007/s10340-022-01549-6