José C. Zanuncio1 Harley N. Oliveira1 Jorge B. Torres2 Dirceu Pratissoli 3
Recibido 18-V-1999. Corregido 26-VII-1999. Aceptado 24-VIII-1999.
Resumen
Huevos de Podisus sculptus Distant (Heteroptera: Pentatomidae) fueron recolectados en una alta población de larvas desfoliadoras de eucalipto, en Almerin, Estado de Pará, Brasil. Se obtuvieron seis especies de parasitóides de esos huevos: Ooencyrtus submetallicus Howard, Ooencyrtus sp.1 y sp.2 (Hymenoptera: Encyrtidae), Telenomus persimilis Ashmead, Telenomus cristatus Johnson y Trissolcus pustulans Johnson (Hymenoptera: Scelionidae). T. persimilis presentaron una mayor tasa de parasitismo en huevos de P. sculptus. Además, esta espécie y O. submetallicus presentaron la mayor tasa de parasitismo de huevos de hospedeiro alternativo Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) en laboratorio.
]]>
predator, parasitoids, biological control.
Pentatomidae predators, particularly of the genus Podisus, have been reported as natural enemies of many insect pests in North America (McPherson 1980). In Brazil, they have been registered in plantations of Eucalyptus (Zanuncio et al. 1994b), Pinus (Teixeira and Villa 1987), soybean and cotton (Grazia and Hildebrand 1987), coffee (Gravena and Lara 1982), cashew (Silva 1965), passion fruit (Costa Lima 1940), avocado (Fischer and Patel 1989) and beans (Jacomino et al.1989). For this reason, species of this group are important as biological control agents of many species of defoliator caterpillars and other insects, both in natural occurrence and in programmed releases (Zanuncio et al. 1994a).
Species of predatory bugs of the genus Podisus present wide distribution and can be found in most Brazilian States such as Goiás (Zanuncio et al. 1991), Ceará (Silva 1965), Mato Grosso do Sul (Jacomino et al.1989), Pará (Zanuncio et al.1993), Rio Grande do Sul (Gastal 1981), São Paulo (Teixeira and Villa 1987), Espírito Santo (Moraes et al. 1983), Rio de Janeiro (Guajará et al. 1993) and Minas Gerais (Zanuncio et al.1994a). Grazia and Hildebrand (1987) consider that Podisus nigrispinus Dallas, Podisus cloelia Stal, Podisus sagitta Fab. (=P. nigrispinus), Podisus thetis Stal and Podisus volxemi are the most common species of this group in Brazil.Although P. nigrispinus and Brontocoris tabidus Signoret are the best known Pentatomidae predators in Brazil (Zanuncio et al. 1992), other species of this genus, Podisus sculptus Distant is found in the State of Pará, Brazil and in Costa Rica, Panama, Peru and Bolivia (Thomas 1992).
Few species of Pentatomidae predatory species have been used in biological control programs in Brazil, mainly due to the limited knowledge of their predatory habits and biology as well as techniques of mass rearing, liberation, evaluation and management after release (Torres et al. 1996). Populations of these predators in the agroecosystems can be affected by factors such as prey availability (O'Neil and Stimac 1988), prey defense (Tostowaryk 1972), parasitoids and predators (Torres et al. 1997). Knowledge of these factors is important to estimate population tendencies and potential of these controllers (Luck et al.1988).
Egg parasitoids of Pentatomidae of the Scelionidae, Encyrtidae, Trichogrammatidae and those of 13 other families (Lassale and Gauld 1993) are important agents of biological control due to their great diversity and high mortality caused to their hosts (Orr et al. 1986). Species of Scelionidae can affect biological control programs because they can parasite eggs of native and introduced Pentatomidae predators and phytophagous species of this family (Orr 1988).
Johnson (1984, 1985) reported that Trissolcus basalis Wollaston, Trissolcus solocis, Trissolcus cristatus Johnson and Telenomus hullensis parasitized Podisus maculiventris Say. Orr et al.(1986) mention that T. basalis, Trissolcus euchisti Asmead, Trissolcus edessae, Telenomus cristatus Johnson and Telenomus podisi Ashmead parasitized eggs of P. maculiventris in soybeans fields in the United States. Torres et al. (1996) indicated the occurrence of T. podisi, Trissolcus brochymenae Ashmead, Ooencyrtus sp., Anastatus spp. and Trissolcus scuticarinatus in eggs of P.nigrispinus collected in plantations of Eucalyptus cloeziana in the State of Minas Gerais, Brazil and Barcelos et al. (1994) found eggs of B. tabidus parasited by T. cristatus and T. brochymenae.
Considering that egg parasitoids can have a great impact on populations of Pentatomidae predators the objective of this research was to identify egg parasitoids of P. sculptus collectedin the County of Almerim, State of Pará, Brazil in an outbreak of the Eucalyptus defoliator species Thyrinteina arnobia Stoll(Lepidoptera: Geometridae), Sarsina violascens Herrich-Schaeffer(Lepidoptera: Lymantridae) and Nystalea nyseus Cramer (Lepidoptera: Notodontidae).
Egg masses of P. sculptus were collected in plants of Eucalyptus urophylla and transported to the Laboratory of Entomology, of the "Universidade Federal de Viçosa (UFV)", in Viçosa, State of Minas Gerais, Brazil. These egg masses were individualized in Petri dishes (9.0 cm diameter and 1.5 cm height) at a temperature of 25.0 ± 1.0 ºC, relative humidity of 60.0 ± 10.0% and a photoperiod of 12 hours where they were observed twice a day to check for nymph hatching and emergence of egg parasitoids. All nymphs of P. sculptus were removed and the remaining predator eggs were placed in glass tubes with honey and capped with cotton, to evaluate the rate of parasitism. ]]>
Six parasitoid species were obtained from egg masses of P. sculptus: Ooencyrtus submetallicus Howard, Ooencyrtus sp.1 and Ooencyrtus sp.2 (Hymenoptera: Encyrtidae), and T. cristatus, Trissolcus pustulans (Johnson) and Telenomus persimilis Ashmead (Hymenoptera: Scelionidae). The last species presented the highest parasitism rate in eggs of P.sculptus and has also been reported as T. podisi (Johnson 1984).T. persimilis and another species, O. submetallicus, showed higher parasitism rate of eggs of the alternative host P. nigrispinus, in laboratory, while the other species did not present good development in this host. This suggests that T. persimilis and O. submetallicus can have a larger impact on populations of Pentatomidae predatory species, because they are not specific. This could allow them to maintain their populations in Eucalyptus plantations when the host P. sculptus is at low population numbers.
Acknowledgements
We thank Dr. Norman F. Johnson (Ohio State University) for the identification of the egg parasitoid species. We also thank the "Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)"; the "Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)" and the "Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)" for grants.
References
Barcelos, J.A.V., Zanuncio, J.C., Oliveira, A.C. & Nascimento, E.C. 1994. Performance em duas dietas e descrição dos adultos de Brontocoris tabidus (Signoret) (Heteroptera: Pentatomidae). An. Soc. Entomol. Bras. 23: 519-524. [ Links ]
Costa Lima, A. 1940. Insetos do Brasil, 2º tomo, Hemípteros. Escola Nacional de Agronomia, RJ, 351p. (Série Didática nº 3). [ Links ]
Fischer, H.Z. & Patel, P.N. 1989. Flutuação populacional da entomofauna e interação de alguns lepidópteros pragas potenciais do abacateiro com seus inimigos naturais. In: CONGRESSO BRASILEIRO DE ENTOMOLOGIA, 12, Belo Horizonte, 1989. Resumos... Belo Horizonte, Sociedade Entomológica do Brasil, p.120. [ Links ]
Gastal, H.A.O. 1981. Lista preliminar dos Asopinae (Hemiptera: Pentatomidae) do Estado do Rio Grande do Sul (Brasil). Iheringia. 57: 119-127, 1981. (Série Zoológica). [ Links ]
Gravena, S. & Lara, F.M. 1982. Controle integrado de pragas e receituário agronômico. In: GRAZIANO NETO. Receituário agronômico. São Paulo, Agroedições, p. 123-161. [ Links ]
Grazia, J. & Hildebrand, R. 1985. Hemipteros predadores de insetos. In: ENCONTRO SUL BRASILEIRO DE CONTROLE DE PRAGAS. I, Passo Fundo, 1985. Anais... Passo Fundo, AEAPF-CNPT/EMBRAPA, 1987. p. 21-37. [ Links ]
Guajará, M.S., Lima, A.F., Racca Filho, F. & Almeida, M.A. 1993. Insetos associados à Eucalyptus spp. no campus da U.F.R.R.J. In: CONGRESSO BRASILEIRO DE ENTOMOLOGIA, 14, Piracicaba, 1993. Resumos... Piracicaba, Sociedade Entomológica do Brasil, 1993. p. 668. [ Links ]
Jacomino, A.P., Cristan, C.A., Boiça Jr., A.L. & Bolonhezi, A.C. 1989. Insetos-praga e seus inimigos naturais amostrados em diversas espécies de leguminosas em "adubação verde", cultivadas na região de Selvíria-MS. In: CONGRESSO BRASILEIRO DE ENTOMOLOGIA, 12, Belo Horizonte, 1989. Resumos... Belo Horizonte, Sociedade Entomológica do Brasil, 1989. p. 78. [ Links ]
Johnson, N.F. 1984. Revision of the Neartic species of the Trissolcus flavipes group (Hymenoptera: Scelionidae). Proc. Entomol. Soc. Wash. 86: 797-807. [ Links ]
Johnson, N.F. 1985. Systematics of new world Trissolcus (Hymenoptera: Scelionidae): species related to T. basalis. Can. Entomol., 117: 431-445. [ Links ]
Lasalle, J. & Gauld, I.D. 1993. Hymenoptera: their diversity, and their impact on the diversity of other organisms. In: LASALLE, J. & GAULD, I.D. Hymenoptera and biodiversity. London, C.B.A. International, 348p. [ Links ]
Luck, R.F., Shepard, B.M. & Kenmore, P.E. 1988. Experimental methods for evaluating arthropod natural enemies. Ann. Rev. Entomol., 33: 367-391. [ Links ]
McPherson, J.E. 1980. A list of prey species of Podisus maculiventris (Hemiptera: Pentatomidae). Great Lakes Ent. 13: 17-24. [ Links ]
Moraes, G.W.G., Brun, P.G., Teixeira, V.S. & Soares, L.A. 1983. O controle biológico dos lepidópteros desfolhadores de eucaliptos em Minas Gerais. Inf. Agrop., 9: 23-30. [ Links ]
O’Neil, R.J. & Stimac, J.L. 1988. Measurement and analysis of arthropod predation on velvetbean caterpillar, Anticarsia gemmatalis Hubner, in soybean. Environ. Entomol., 17: 987-993. [ Links ]
Orr, D.B. 1988. Scelionid wasp as biological control agents: a review. Fl. Entomol., 71: 505-528. [ Links ]
Orr, D.B., Russin, J.S. & Boethel, D.J. 1986. Reproductive biology behavior of Telenomus calvus (Hymenoptera: Scelionidae), a phoretic egg parasitoid of Podisus maculiventris (Hemiptera: Pentatomidae). Can. Entomol., 118: 1063-1072. [ Links ]
Silva, A.F. 1965. Notas sobre Podisus nigrolimbatus (Spinola, 1852) (Pentatomidae: Asopinae). Bol. Soc. Agron. 6: 27-28. [ Links ]
Teixeira, E.P. & Villa, W.M. 1987. Associação de lagartas (Lepidoptera: Geometridae) dessaciculadoras de Pinus patula Sche & Chan em Itararé. São Paulo. I. Aspectos parasitológicos. In: CONGRESSO BRASILEIRO DE ENTOMOLOGIA, 11, Campinas, 1987. Resumos... Campinas, Fundação Cargil, p. 389. [ Links ]
Thomas, D.B. 1992. Taxonomic synopsis of the Asopinae Pentatomidae (Heteroptera) of the Western Hemisphere. Maryland Entomological Society of America. 147p. (Thomas Say Foundation Monography). [ Links ]
Torres, J.B., Zanuncio, J.C., Cecon, P.R. & Gasperazzo, W.L. 1996. Mortalidade de Podisus nigrispinus (Dallas) por parasitóides de ovos em áreas de eucalipto. An. Soc. Entomol. Bras., 25: 463-472. [ Links ]
Torres, J.B., Pratissoli, D. & Zanuncio, J.C. 1997. Exigências térmicas e potencial de desenvolvimento dos parasitóides Telenomus podisi Ashmead e Trissolcus brochymenae (Ashmead) em ovos do percevejo depredador Podisus nigrispinus (Dallas). An. Soc. Entomol. Bras., 26: 445-454. [ Links ]
Tostowaryk, W. 1972. The effect of prey defense on the functional response of Podisus modestus (Hemiptera: Pentatomidae) to densities of the sawflies Neodiprion swainei and N. prati banksiane (Hymenoptera: Neodiprionidae). Can. Entomol., 104: 61-69. [ Links ]
Zanuncio, J.C., Nascimento, E.C., Santos, G.P., Sartório, R.C. & Araújo, F.S. 1991. Aspectos biológicos do percevejo depredador Podisus connexivus Bergroth, 1891 (Hemiptera: Pentatomidae). An. Soc. Entomol. Bras., 20: 243-249. [ Links ]
Zanuncio, J.C., Alves, J.B., Leite, J.E.M. & Sartório, R.C. 1992. Métodos para criação de hemípteros predadores de lagartas. An. Soc. Entomol. Bras., 21: 245-251. [ Links ]
Zanuncio, J.C., Nascimento, E.C., Zanuncio, T.V. & Cruz, A.P. 1993. Descrição das ninfas do depredador Podisus sculptus Distant, 1889 (Hemiptera: Pentatomidae). R. bras. Entomol., 37: 403-408. [ Links ]
Zanuncio, J.C., Alves, J.B., Zanuncio, T.V. & Garcia, J.F. 1994a. Hemipterous predators of eucalypt defoliator caterpillars. For. Ecol. Manag., 65: 65-73. [ Links ]
Zanuncio, J.C., Nascimento, E.C., Garcia, J.F. & Zanuncio T.V. 1994b. Major lepidopterous defoliators of eucalypt, in the southeast region of Brazil. For. Ecol. Manag., 65: 53-63. [ Links ]
1 Departamento de Biologia Animal, Universidade Federal de Viçosa. 36571-000 Viçosa, Minas Gerais, Brasil. e-mail: zanuncio@mail.ufv.br
2 DEPA-Fitossanidade, Universidade Federal Rural de Pernambuco. 52171-000 Recife, Pernambuco, Brasil.
3 Centro Agropecuário da Universidade Federal do Espírito Santo. 29360-000 Alegre, Espírito Santo, Brasil.
]]>