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Occurrence of Dinarmus basalis parasitizing Callosobruchus maculatus in Vigna unguiculata in the semiarid region of the Rio Grande do Norte state, Brazil

Ocorrência de Dinarmus basalis parasitando Callosobruchus maculatus em Vigna unguiculata no semiárido do Rio Grande do Norte, Brasil

ABSTRACT

Callosobruchus maculatus (Fab.) (Coleoptera: Chrysomelidae: Bruchinae) is the main pest of Vigna unguiculata (L.) Walp. during the grain storage period. This study aimed to report the occurrence of a natural enemy associated with C. maculatus in cowpea, in the semiarid region of the Rio Grande do Norte state, Brazil. For this, cowpea samples were collected and placed in closed plastic containers, where they remained until the emergence of adult insects. From the infested samples, adults of C. maculatus and of the Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae: Pteromalinae) parasitoid emerged. This is the first report of D. basalis parasitizing C. maculatus in the semiarid region of the Rio Grande do Norte state.

KEYWORDS:
Cowpea; Bruchinae; Pteromalidae; biological control

RESUMO

Callosobruchus maculatus (Fab.) (Coleoptera: Chrysomelidae: Bruchinae) é a principal praga de Vigna unguiculata (L.) Walp. durante o período de armazenamento dos grãos. Objetivou-se relatar a ocorrência de um inimigo natural associado a C. maculatus em feijão-caupi, na região semiárida do Rio Grande do Norte, Brasil. Para isso, amostras de feijão-caupi foram coletadas e colocadas em recipientes plásticos fechados, onde permaneceram até a emergência dos insetos adultos. Das amostras infestadas, emergiram adultos de C. maculatus e do parasitoide Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae: Pteromalinae). Este é o primeiro relato de D. basalis parasitando C. maculatus na região semiárida do Rio Grande do Norte.

PALAVRAS-CHAVE:
Feijão-caupi; Bruchinae; Pteromalidae; controle biológico

Callosobruchus maculatus (Fab.) (Coleoptera: Chrysomelidae: Bruchinae) is the main pest of Vigna unguiculata (L.) Walp. cowpea during the grain storage period (Heidari et al. 2016HEIDARI, N.; SEDARATIAN-JAHROMI, A.; GHANE-JAHROMI, M. Possible effects of ultraviolet ray (UV-C) on biological traits of Callosobruchus maculatus (Col.: Chrysomelidae). Journal of Stored Products Research, v. 69, n. 1, p. 91-98, 2016., Medeiros et al. 2017MEDEIROS, W. R.; SILVA, J. D. C.; SILVA, P. R. R.; GIRÃO FILHO, J. E.; PADUA, L. E. M.; FRANÇA, S. M. Resistência de genótipos de feijãocaupi [Vigna unguiculata (L.) Walp.] ao ataque do caruncho Callosobruchus maculatus (Fabr.) (Coleoptera: Chrysomelidae). EntomoBrasilis, v. 10, n. 1, p. 19-25, 2017., Silva et al. 2020SILVA, A. B.; OLIVEIRA, C. R. F.; MATOS, C. H. C.; SANTOS, P. E. M.; LIRA, C. R. I. M. Bioatividade do óleo essencial de Croton blanchetianus Baill (Euphorbiaceae) sobre Callosobruchus maculatus Fabricius, 1775 (Coleoptera: Chrysomelidae). Nativa, v. 8, n. 4, p. 450-455, 2020.). The damage related to the attack of this pest is due to the penetration and feeding of the larvae inside the grains, affecting their commercial and agronomic quality and making them unsuitable for human consumption and sowing (Oliveira et al. 2014OLIVEIRA, G. B.; KUNZ, D.; PERES, T. V.; LEAL, R. B.; UCHÔA, A. F.; SAMUELS, R. I.; MACEDO, M. L. R.; CARLINI, C. R.; RIBEIRO, A. F.; GRANGEIRO, T. B.; TERRA, W. R.; XAVIER-FILHO, J.; SILVA, C. P. Variant vicilins from a resistant Vigna unguiculata lineage (IT81D-1053) accumulate inside Callosobruchus maculatus larval midgut epithelium. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, v. 168, n. 1, p. 45-52, 2014.).

The main method to control C. maculatus is chemical control with synthetic insecticides (e.g., organophosphates, pyrethroids and phosphine) (Gusmão et al. 2013GUSMÃO, N. M. S.; OLIVEIRA, J. V.; NAVARRO, D. M. A. F.; DUTRA, K. A.; SILVA, W. A.; WANDERLEY, M. J. A. Contact and fumigant toxicity and repellency of Eucalyptus citriodora Hook., Eucalyptus staigeriana F., Cymbopogon winterianus Jowitt and Foeniculum vulgare Mill. essential oils in the management of Callosobruchus maculatus (FABR.) (Coleoptera: Chrysomelidae, Bruchinae): a review. Journal of Stored Products Research, v. 54, n. 1, p. 41-47, 2013.). In Brazil, the number of insecticides registered for the control of C. maculatus in cowpea is limited, being restricted to magnesium phosphide (Brasil 2003BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Agrofit. 2003. Available at: https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Access on: Aug. 02, 2023.
https://agrofit.agricultura.gov.br/agrof...
). However, the inappropriate use of these insecticides can cause several problems, e.g., intoxication of rural workers, residue accumulation in grains and emergence of resistant pest populations, among others (Pimentel et al. 2010PIMENTEL, M. A. G.; FARONI, L. R. D. A.; SILVA, F. H.; BATISTA, M. D.; GUEDES, R. N. C. Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotropical Entomology, v. 39, n. 1, p. 101-107, 2010., Hedjal-Chehheb et al. 2013HEDJAL-CHEHHEB, M.; TOUDERT-TALEB, K.; KHOUDJA, M. L.; BENABDESSELAM, R.; MELLOUK, M.; KELLOUCHE, A. Essential oils compositions of six conifers and their biological activity against the cowpea weevil, Callosobruchus maculatus Fabricius, 1775 (Coleoptera: Bruchidae) and Vigna unguiculata seeds. African Entomology, v. 21, n. 2, p. 243-254, 2013.).

Thus, the use of botanical insecticides (Hedjal-Chehheb et al. 2013HEDJAL-CHEHHEB, M.; TOUDERT-TALEB, K.; KHOUDJA, M. L.; BENABDESSELAM, R.; MELLOUK, M.; KELLOUCHE, A. Essential oils compositions of six conifers and their biological activity against the cowpea weevil, Callosobruchus maculatus Fabricius, 1775 (Coleoptera: Bruchidae) and Vigna unguiculata seeds. African Entomology, v. 21, n. 2, p. 243-254, 2013., Izakmehri et al. 2013IZAKMEHRI, K.; MOOSA, S.; MEHRVAR, S.; HASSANPOURAGHDAM, M. B.; VOJOUDI, S. Lethal and sublethal effects of essential oils from Eucalyptus camaldulensis and Heracleum persicum against the adults of Callosobruchus maculatus. Journal of Insect Science, v. 13, n. 1, p. 1-10, 2013., Mbata & Payton 2013MBATA, G. N.; PAYTON, M. E. Effect of monoterpenoids on oviposition and mortality of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) under hermetic conditions. Journal of Stored Products Research, v. 53, n. 1, p. 43-47, 2013., Sousa Neto et al. 2019SOUSA NETO, E. P.; ANDRADE, A. B. A.; COSTA, E. M.; MARACAJÁ, P. B.; SANTOS, A. B.; SANTOS, J. L. G.; PIMENTA, T. A. Effect of neem powder (Azadirachta indica A. Juss) on the control of cowpea weevils [Callosobruchus maculatus (F.) (Coleoptera: Bruchidae)] in cowpea beans. Journal of Experimental Agriculture International, v. 30, n. 2, p. 1-7, 2019.) and biological control with parasitoids (Amevoin et al. 2007AMEVOIN, K.; SANON, A.; APOSSABA, M.; GLITHO, I. A. Biological control of bruchids infesting cowpea by the introduction of Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) adults into farmers’ stores in west Africa. Journal of Stored Products Research, v. 43, n. 3, p. 240-247, 2007.) have been studied as alternatives to synthetic insecticides. Several parasitoids associated with C. maculatus have been reported worldwide, with the Pteromalidae family being the most diversified, with five species distributed in the genera Dinarmus, Theocolax and Lariophagus (Van Huis 1991VAN HUIS, A. Biological methods of bruchid control in the tropics: a review. International Journal of Tropical Insect Science, v. 12, n. 3, p. 87-102, 1991.). In a study carried out in west Africa, Amevoin et al. (2007)AMEVOIN, K.; SANON, A.; APOSSABA, M.; GLITHO, I. A. Biological control of bruchids infesting cowpea by the introduction of Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) adults into farmers’ stores in west Africa. Journal of Stored Products Research, v. 43, n. 3, p. 240-247, 2007. reported that, after the parasitoid Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) was released, a significant reduction in the populations of C. maculatus in stored cowpea was observed, consequently resulting in lower losses, when compared to the control treatment.

In Brazil, information about the occurrence of natural enemies of the Callosobruchus genus is still scarce, with records in the states of Santa Catarina (Lima 1942LIMA, A. D. F. Mais um inimigo do Callosobruchus chinensis. Boletim da Sociedade Brasileira de Agronomia, v. 5, n. 1, p. 441-443, 1942.), Pará (Ohashi et al. 1993OHASHI, O. S.; COUTINHO, J. C. B.; SILVA, O. F. Aspectos biológicos de Dinarmus basalis (Rondani, 1877) (Hymenoptera: Pteromalidae) ectoparasito de Callosobruchus maculatus (Fabricius, 1775) (Coleoptera: Bruchidae). Anais da Sociedade Entomológica do Brasil, v. 22, n. 1, p. 161-167, 1993.) and São Paulo (Costa et al. 2007COSTA, V. A.; GUZZO, E. C.; LOURENÇÃO, A. L.; TAVARES, M. A. G. C.; VENDRAMIM, J. D. Occurrence of Dinarmus basalis in Callosobruchus analis in stored soybean in São Paulo, Brazil. Scientia Agricola, v. 64, n. 3, p. 301-302, 2007.). Therefore, this study aimed to report, for the first time, the occurrence of a parasitoid associated with C. maculatus in cowpea, in the semiarid region of the Rio Grande do Norte state, Brazil.

A total of 20 cowpea samples of 200 g from the Mossoró region (5º11’S and 37º20’W) were taken to the laboratory at the Universidade Federal Rural do Semiárido, in 2013, where they were placed in plastic containers (6 cm high × 10 cm in diameter) closed at the top with voile fabric and kept in an air-conditioned room (25 ± 2 ºC; 70 ± 10 % RH; 12-h photoperiod). The cowpea samples were inspected daily until the emergence of C. maculatus adults (± 20 days after collection) or parasitoids. Subsequently, the obtained insects were transferred to containers with 70 % ethyl alcohol and duly labelled (date and sampling location). The emerged parasitoids were identified according to Bouček & Heydon (1997)BOUČEK, Z.; HEYDON, S. L. Pteromalidae. In: GIBSON, G. A. P.; HUBER, J. T.; WOOLLEY, J. B. Annotated keys to the genera of Nearctic chalcidoidea (Hymenoptera). Ottawa: NRC Research Press, 1997. p. 541-692. for genus and Rasplus (1989)RASPLUS, J. Y. Révision des espèces afrotropicales du genre Dinarmus Thomson (Hymenoptera: Pteromalidae). Annales de la Société Entomologique de France, v. 25, n. 1, p. 135-162, 1989. for species. The Bruchinae specimens were sent to the Universidade Federal Rural de Pernambuco (UFRPE), in Recife, Pernambuco state, Brazil, for identification. The voucher specimens of the parasitoid were deposited in the entomological collection of the Instituto Biológico of São Paulo, whereas the C. maculatus specimens were deposited in the entomological collection of the UFRPE.

A total of 2,083 insects were collected from the cowpea samples, with 1,414 C. maculatus and 669 parasitoids belonging to Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) (Figure 1). This parasitoid is a solitary idiobiont ectoparasitoid of immature insects and may be used for the biological control of C. maculatus (Amevoin et al. 2007AMEVOIN, K.; SANON, A.; APOSSABA, M.; GLITHO, I. A. Biological control of bruchids infesting cowpea by the introduction of Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) adults into farmers’ stores in west Africa. Journal of Stored Products Research, v. 43, n. 3, p. 240-247, 2007.). This parasitoid is the main natural enemy of bruchids in cowpea grains (Sanon et al. 2011SANON, A.; BA, M. N.; DABIRÉ, L. C. B.; NÉBIÉ, R. C. H.; MONGE, J. P. Side effects of grain protectants on biological control agents: how Hyptis plant extracts affect parasitism and larval development of Dinarmus basalis. Phytoparasitica, v. 39, n. 3, p. 215-222, 2011.). Dinarmus basalis is originally from Africa and has dispersed throughout the Americas, Asia and Europe due to the trade in grains and seeds (Rasplus 1989RASPLUS, J. Y. Révision des espèces afrotropicales du genre Dinarmus Thomson (Hymenoptera: Pteromalidae). Annales de la Société Entomologique de France, v. 25, n. 1, p. 135-162, 1989.).

Figure 1
Female of Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) collected in Mossoró, Rio Grande do Norte state, Brazil.

In Brazil, D. basalis has already been reported parasitizing Callosobruchus chinensis (L.) associated with Vigna radiata (L.) in the Santa Catarina state (Lima 1942LIMA, A. D. F. Mais um inimigo do Callosobruchus chinensis. Boletim da Sociedade Brasileira de Agronomia, v. 5, n. 1, p. 441-443, 1942.), Acanthoscelides obtectus (Say) in the Northeast region of Brazil (Oliveira 1948OLIVEIRA, M. A. Contribuição ao estudo do combate biológico do gorgulho do feijão (Acanthoscelides obsoletus Say) pelo Bruchobius laticeps Ash. Agros, v. 1, n. 1, p. 258-268, 1948.), C. maculatus associated with V unguiculata in the Pará state (Ohashi et al. 1993OHASHI, O. S.; COUTINHO, J. C. B.; SILVA, O. F. Aspectos biológicos de Dinarmus basalis (Rondani, 1877) (Hymenoptera: Pteromalidae) ectoparasito de Callosobruchus maculatus (Fabricius, 1775) (Coleoptera: Bruchidae). Anais da Sociedade Entomológica do Brasil, v. 22, n. 1, p. 161-167, 1993.) and Callosobruchus analis (F.) associated with Glycine max (L.) in the São Paulo state (Costa et al. 2007COSTA, V. A.; GUZZO, E. C.; LOURENÇÃO, A. L.; TAVARES, M. A. G. C.; VENDRAMIM, J. D. Occurrence of Dinarmus basalis in Callosobruchus analis in stored soybean in São Paulo, Brazil. Scientia Agricola, v. 64, n. 3, p. 301-302, 2007.). However, this is the first report of D. basalis parasitizing C. maculatus associated with cowpea in the semiarid region of the Rio Grande do Norte state, Brazil.

REFERENCES

  • AMEVOIN, K.; SANON, A.; APOSSABA, M.; GLITHO, I. A. Biological control of bruchids infesting cowpea by the introduction of Dinarmus basalis (Rondani) (Hymenoptera: Pteromalidae) adults into farmers’ stores in west Africa. Journal of Stored Products Research, v. 43, n. 3, p. 240-247, 2007.
  • BOUČEK, Z.; HEYDON, S. L. Pteromalidae. In: GIBSON, G. A. P.; HUBER, J. T.; WOOLLEY, J. B. Annotated keys to the genera of Nearctic chalcidoidea (Hymenoptera). Ottawa: NRC Research Press, 1997. p. 541-692.
  • BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Agrofit 2003. Available at: https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons Access on: Aug. 02, 2023.
    » https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons
  • COSTA, V. A.; GUZZO, E. C.; LOURENÇÃO, A. L.; TAVARES, M. A. G. C.; VENDRAMIM, J. D. Occurrence of Dinarmus basalis in Callosobruchus analis in stored soybean in São Paulo, Brazil. Scientia Agricola, v. 64, n. 3, p. 301-302, 2007.
  • GUSMÃO, N. M. S.; OLIVEIRA, J. V.; NAVARRO, D. M. A. F.; DUTRA, K. A.; SILVA, W. A.; WANDERLEY, M. J. A. Contact and fumigant toxicity and repellency of Eucalyptus citriodora Hook., Eucalyptus staigeriana F., Cymbopogon winterianus Jowitt and Foeniculum vulgare Mill. essential oils in the management of Callosobruchus maculatus (FABR.) (Coleoptera: Chrysomelidae, Bruchinae): a review. Journal of Stored Products Research, v. 54, n. 1, p. 41-47, 2013.
  • HEDJAL-CHEHHEB, M.; TOUDERT-TALEB, K.; KHOUDJA, M. L.; BENABDESSELAM, R.; MELLOUK, M.; KELLOUCHE, A. Essential oils compositions of six conifers and their biological activity against the cowpea weevil, Callosobruchus maculatus Fabricius, 1775 (Coleoptera: Bruchidae) and Vigna unguiculata seeds. African Entomology, v. 21, n. 2, p. 243-254, 2013.
  • HEIDARI, N.; SEDARATIAN-JAHROMI, A.; GHANE-JAHROMI, M. Possible effects of ultraviolet ray (UV-C) on biological traits of Callosobruchus maculatus (Col.: Chrysomelidae). Journal of Stored Products Research, v. 69, n. 1, p. 91-98, 2016.
  • IZAKMEHRI, K.; MOOSA, S.; MEHRVAR, S.; HASSANPOURAGHDAM, M. B.; VOJOUDI, S. Lethal and sublethal effects of essential oils from Eucalyptus camaldulensis and Heracleum persicum against the adults of Callosobruchus maculatus. Journal of Insect Science, v. 13, n. 1, p. 1-10, 2013.
  • LIMA, A. D. F. Mais um inimigo do Callosobruchus chinensis. Boletim da Sociedade Brasileira de Agronomia, v. 5, n. 1, p. 441-443, 1942.
  • MBATA, G. N.; PAYTON, M. E. Effect of monoterpenoids on oviposition and mortality of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) under hermetic conditions. Journal of Stored Products Research, v. 53, n. 1, p. 43-47, 2013.
  • MEDEIROS, W. R.; SILVA, J. D. C.; SILVA, P. R. R.; GIRÃO FILHO, J. E.; PADUA, L. E. M.; FRANÇA, S. M. Resistência de genótipos de feijãocaupi [Vigna unguiculata (L.) Walp.] ao ataque do caruncho Callosobruchus maculatus (Fabr.) (Coleoptera: Chrysomelidae). EntomoBrasilis, v. 10, n. 1, p. 19-25, 2017.
  • OHASHI, O. S.; COUTINHO, J. C. B.; SILVA, O. F. Aspectos biológicos de Dinarmus basalis (Rondani, 1877) (Hymenoptera: Pteromalidae) ectoparasito de Callosobruchus maculatus (Fabricius, 1775) (Coleoptera: Bruchidae). Anais da Sociedade Entomológica do Brasil, v. 22, n. 1, p. 161-167, 1993.
  • OLIVEIRA, G. B.; KUNZ, D.; PERES, T. V.; LEAL, R. B.; UCHÔA, A. F.; SAMUELS, R. I.; MACEDO, M. L. R.; CARLINI, C. R.; RIBEIRO, A. F.; GRANGEIRO, T. B.; TERRA, W. R.; XAVIER-FILHO, J.; SILVA, C. P. Variant vicilins from a resistant Vigna unguiculata lineage (IT81D-1053) accumulate inside Callosobruchus maculatus larval midgut epithelium. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, v. 168, n. 1, p. 45-52, 2014.
  • OLIVEIRA, M. A. Contribuição ao estudo do combate biológico do gorgulho do feijão (Acanthoscelides obsoletus Say) pelo Bruchobius laticeps Ash. Agros, v. 1, n. 1, p. 258-268, 1948.
  • PIMENTEL, M. A. G.; FARONI, L. R. D. A.; SILVA, F. H.; BATISTA, M. D.; GUEDES, R. N. C. Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotropical Entomology, v. 39, n. 1, p. 101-107, 2010.
  • RASPLUS, J. Y. Révision des espèces afrotropicales du genre Dinarmus Thomson (Hymenoptera: Pteromalidae). Annales de la Société Entomologique de France, v. 25, n. 1, p. 135-162, 1989.
  • SANON, A.; BA, M. N.; DABIRÉ, L. C. B.; NÉBIÉ, R. C. H.; MONGE, J. P. Side effects of grain protectants on biological control agents: how Hyptis plant extracts affect parasitism and larval development of Dinarmus basalis. Phytoparasitica, v. 39, n. 3, p. 215-222, 2011.
  • SILVA, A. B.; OLIVEIRA, C. R. F.; MATOS, C. H. C.; SANTOS, P. E. M.; LIRA, C. R. I. M. Bioatividade do óleo essencial de Croton blanchetianus Baill (Euphorbiaceae) sobre Callosobruchus maculatus Fabricius, 1775 (Coleoptera: Chrysomelidae). Nativa, v. 8, n. 4, p. 450-455, 2020.
  • SOUSA NETO, E. P.; ANDRADE, A. B. A.; COSTA, E. M.; MARACAJÁ, P. B.; SANTOS, A. B.; SANTOS, J. L. G.; PIMENTA, T. A. Effect of neem powder (Azadirachta indica A. Juss) on the control of cowpea weevils [Callosobruchus maculatus (F.) (Coleoptera: Bruchidae)] in cowpea beans. Journal of Experimental Agriculture International, v. 30, n. 2, p. 1-7, 2019.
  • VAN HUIS, A. Biological methods of bruchid control in the tropics: a review. International Journal of Tropical Insect Science, v. 12, n. 3, p. 87-102, 1991.

Publication Dates

  • Publication in this collection
    20 Oct 2023
  • Date of issue
    2023

History

  • Received
    17 Apr 2023
  • Accepted
    19 July 2023
  • Published
    16 Aug 2023
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