Parasitoides associados com Helicoverpa armigera em áreas de refúgio de algodão, no Oeste da Bahia, Brasil

Luz, Priscila Maria Colombo da; Paula-Moraes, Silvana Vieira de; López, Juan Manuel Perilla; Pujol-Luz, José Roberto; Penteado-Dias, Angélica Maria; Specht, Alexandre; Diniz, Ivone Rezende

doi:10.1590/0103-8478cr20170250

ABSTRACT:

Natural biological control is one of the major causes responsible for reduction of pest population in agricultural ecosystem. However, natural biological control importance is usually minimized by not being estimated. This study reports the occurrence of Campoletis sonorensis (Cameron, 1886) (Hymenoptera: Ichneumonidae), Archytas marmoratus (Townsend, 1915) and Archytas incertus (Macquart, 1851) (Diptera: Tachinidae) associated with Helicoverpa armigera (Hübner, 1809) (Lepidoptera: Noctuidae). The rate of larval parasitism was up to 41% in structured refuge areas of cotton, without chemical control with insecticides. This study strengthens our knowledge relating to parasitoids associated with natural control of H. armigera in the American continent. In addition, it documents the rule that structured refuge areas could play as a source of natural enemies, besides their contribution to production of non-selective populations to Bt technology.

Key words:
biological control; integrated pest management; natural enemies

RESUMO:

O controle biológico natural é um dos principais componentes responsáveis pela redução populacional de pragas em agroecossistemas. Entretanto, a importância do controle biológico natural, usualmente, é minimizada devido não ser estimada. Este estudo documenta a ocorrência de Campoletis sonorensis (Cameron, 1886) (Hymenoptera: Ichneumonidae), Archytas marmoratus (Townsend, 1915) e Archytas incertus (Macquart, 1851) (Diptera: Tachinidae) associados a Helicoverpa armigera (Hübner, 1809) (Lepidoptera: Noctuidae). A taxa de parasitismo larval foi superior a 41% em áreas de refúgio estruturado de algodão, sem uso de inseticidas químicos. Este estudo fortalece o conhecimento relacionado com os parasitoides associados ao controle natural de H. armigera no Continente Americano. Adicionalmente, documenta o efeito que áreas de refúgio estruturado podem desempenhar como fonte de inimigos naturais, além da sua contribuição para produzir insetos não expostos à tecnologia Bt.

Palavras-chave:
controle biológico; manejo integrado de pragas; inimigos naturais

Helicoverpa armigera (Hübner, 1809) (Lepidoptera: Noctuidae: Heliothinae) has great destructive potential with relevant economic impact world wide (MATTHEWS 1999). Although, H. armigera was first reported in Brazil in 2013 (CZEPAK et al. 2013), a subsequent study (SOSA-GÓMEZ et al. 2016) report that the specie was present in the country at least since 2008.

At least 35 parasitoid species were reported as natural enemies of Heliothinae belonging Hymenoptera and Diptera (FATHIPOUR & SEDARATIAN 2013). Beyond the diversity, parasitoid rates recorded in cotton range from 7% (SHEPARD & STERLING 1972) up to 76% (OBOPILE & MOSINKIE 2007).

Several natural enemies can be reported associated with insects in cotton, including some species of parasitoids. However, in the implementation of measures that favor the survival of theses mortality agents in cotton demands documentation of the species associated with key pests (BASTOS & TORRES 2005). The present study reported the occurrence of larval-pupal parasitoids of H. armigera collected in structured refuge areas of cotton in an intensive cotton cropping system in Correntina municipality, Western Bahia, Brazil.

Larvae were sampled in two structured refuge areas (non-Bt cultivar FM982GL), without chemical insecticide control during 2014/2015 and 2015/2016 crop seasons. The larvae were collected manually (n =301) in a random transversal “zigzag” sampling as described by CORRÊA-FERREIRA et al. (2014) and were individually maintained in polyethylene cups (80 ml) with artificial diet (GREENE et al. 1976) until the emergence of moths or parasitoids. All emerged moths were identified as H. armigera comparing their genitalia (HARDWICK 1965, SPECHT et al. 2013). Likewise, the parasitized larvae or pupae were identified as H. armigera comparing the larval and pupal exuvia with reference material of H. armigera and Helicoverpa zea (Boddie, 1850) maintained in the Laboratório de Entomologia (Embrapa Cerrados).

Dipterans were identified according to CURRAN (1928) and GUIMARÃES (1961), and wasps to AGUIRRE et al. (2015) and GOULET et al. (1993). Voucher specimens were housed in the Department of Zoology - Universidade de Brasília (DZUB), and in the Department of Ecology and Evolutionary Biology - Universidade Federal de São Carlos (DCBU).

From the total of H. armigera larvae sampled, 125 (41.52%) insects were parasitized. The wasp Campoletis sonorensis (Cameron, 1886) (Hymenoptera: Ichneumonidae) (Figure.1A), was identified in 7,00% of the caterpillars; Archytas marmoratus (Townsend, 1915) and Archyrtas incertus (Macquart, 1851) (Diptera: Tachinidae) (Figure.1B), were detected in 34.52% of the larvae.

Figure 1
Lateral view: (A) Campoletis soneronsis, female; (B) Archytas marmoratus, male. [scale=5mm].

Campoletis sonorensis, obtained only during the first sampling (2014/2015), is a generalist endoparasitoid with high efficiency in the biological control of several moth pests, including the Americans Heliothinae as Chloridea virescens (Fabricius, 1777) and H. zea (SHELBY et al. 2000). This wasp has been also mentioned parasitizing H. armigera in the Old World (FATHIPOUR & SEDARATIAN 2013).

Archytas marmoratus and A. incertus are morphologically inconspicuous, but had remarkable differences in their post abdomen structures (Figure.2 A-F), as shown by their male genitalia structures (see Figure.2 B-C, and E-F, respectively), and also by their distribution patterns (GUIMARÃES 1961, 1971). Archytas marmoratus is distributed from the South of the United States to the North of Chile and Brazil (RAVLIN & STEHR 1984); A. incertus is recorded from Argentina, Brazil, Chile and Uruguay (GUIMARÃES 1961), parasitizing lepidopteran pests including: C. virescens, H. zea, and Helicoverpa gelotopoeon (Dyar 1921) (SANCHEZ & RAVEN 1989). This is the first register of A. incertus as parasitoid on H. armigera in Brazil.

Figure 2
Male terminalia - Archytas marmoratus, (A) fifth sternite (ventral view), (B) genital complex (lateral view), (C) surstylus and cercus (posterior view); Archytas incertus, (D) fifth sternite (ventral view), (E) genital complex (lateral view), (F) surstylus and cercus (posterior view).

The close relationship of the Archytas species with Heliothinae (e.g. RAVLIN & STEHR 1984; CARPENTER & PROSHOLD 2000), includes its association with H. armigera, now present in the Americas. Helicoverpa armigera parasitism rate reached a 40%, which could be considered a high natural mortality factor amidst the intensive cropping system of cotton in West Bahia. Parasitoids’ diversity and the high incidence of parasitism detected in structured refuge areas of cotton, without chemical control with insecticide, represents strategic information for the management of H. armigera. These results agreed with OBOPILE & MOSINKIE (2007) who reported 76% parasitism of H. armigera on unsprayed crops in Botswana. Moreover, these results indicated the potential of refuge areas to promote non-selected populations of lepidopteran pests to Bt technology, as well as a way to promote a source of natural enemies in the agricultural landscape of intensive cropping system. Considering the pest pressure in refuge areas in tropical region, an eventual adoption of chemical control with insecticides in structured refuges should be based on selective products (SHEPARD & STERLING 1972; BASTOS & TORRES 2005).

ACKNOWLEDGEMENTS

To Vander Célio Matos Claudino for his help in the field work. To the Panorama farm, Correntina, Bahia, Brazil for providing the sampling areas. To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (proc n◦. 403376/2013-0, 47304/2013-8, 308247/2013-2) and Embrapa (MP2 02.13.14.006.00.00) for research funding. To ICMBio - IBAMA - MMA for the Authorization for scientific activities SISBIO 38547/(1-6).

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» https://doi.org/10.1590%2Fs0100-204x201300060 0015

0
CR-2017-0250.R1

Publication Dates

Publication in this collection
2018

History

Received
11 Apr 2017
Accepted
20 Oct 2017
Reviewed
27 Nov 2017

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] AGUIRRE, H. et al. An illustrated key to Neotropical species of the genus Meteorus Haliday (Hymenoptera, Braconidae, Euphorinae). Zoo Keys, v.489, p.33-94, 2015. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395838/>. Accessed: Sept. 10, 2016. doi: 10.3897/zookeys.489.9258.
» https://doi.org/10.3897/zookeys.489.9258.» https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395838/

[2] BASTOS, C.S.; TORRES, J.B. Controle biológico e o manejo de pragas do algodoeiro. Campina Grande, Embrapa Algodão, 2005, 63p. (Circular Técnica, 72).

[3] CARPENTER, J.E.; PROSHOLD, F.I. Survival of Archytas marmoratus (Diptera: Tachinidae) from superparasitized corn earworm larvae (Lepidoptera: Noctuidae). Environmental Entomology, v.29, p.606-611, 2000. Available from: https://doi.org/10.1603/0046-225X-29.3.606> Accessed: Oct. 20, 2016. doi: 10.1603/0046-225X-29.3.606.
» https://doi.org/10.1603/0046-225X-29.3.606.» https://doi.org/10.1603/0046-225X-29.3.606

[4] CORRÊA-FERREIRA, B.S. et al. Inimigos naturais de Helicoverpa armigera em soja. Londrina, Embrapa soja, 2014, 12p. (Comunicado Técnico 80).

[5] CURRAN, C.H. Revision of the American species of Archytas (Tachinidae, Diptera). The Canadian Entomologist, v.60, p.218-226, 1928. Available from: https://doi.org/10.4039/Ent60 275-11.>. Accessed: Oct. 18, 2016. doi:10.4039/Ent60 275-11.
» https://doi.org/10.4039/Ent60 275-11.

[6] CZEPAK, C. et al. Primeiro registro de ocorrência de Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) no Brasil. Pesquisa Agropecuária Tropical. v.43, p. 110-113, 2013. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1983-40632013000100015&lng=en&nrm=iso>. Accessed: Jan. 18, 2016. doi: 10.1590/S1983-40632013000100015.
» https://doi.org/10.1590/S1983-40632013000100015.» http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1983-40632013000100015&lng=en&nrm=iso

[7] FATHIPOUR, Y.; SEDARATIAN, A. Integrated management of Helicoverpa armigera in soybean cropping systems. In: EL-SHEMY, H.A. (ed.) Soybean-pest Resistance. Cairo, InteOpP, 2013. Cap 9, p. 231-280.Available from: https://doi.org/10.5772/54522>. Accessed: Sept. 19, 2016. doi: 10.5772/54522.
» https://doi.org/10.5772/54522.» https://doi.org/10.5772/54522

[8] GOULET, H.; HUBER, J.T. Hymenoptera of the world: an identification guide to families. Ottawa, Research Branch Agriculture Canada, 1993. Available from: https://doi.org/10.1002%2Fmmnd.19950420212>. Accessed: Oct. 9, 2016. doi: 10.1002/mmnd.19950420212.
» https://doi.org/10.1002/mmnd.19950420212.» https://doi.org/10.1002%2Fmmnd.19950420212

[9] GREENE, G.L. et al. Velvetbean caterpillar: a rearing procedure and artificial medium. Journal of Economic Entomology, v.69, p.488-497, 1976. Available from: https://doi.org/10.1093/jee/69.4.487>. Accessed: Nov. 5, 2016. doi: 10.1093/jee/69.4.487.
» https://doi.org/10.1093/jee/69.4.487.» https://doi.org/10.1093/jee/69.4.487

[10] GUIMARÃES, J.H. Segunda contribuição ao conhecimento do gênero Archytas Jaennecke, 1867 (Diptera: Tachinidae). Memórias do Instituto Oswaldo Cruz, v.59, p. 163-179, 1961. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0074-02761961000200004&lng=en&nrm=iso>. Accessed: Oct. 13, 2016. doi: 10.1590/S0074-02761961000200004.
» https://doi.org/10.1590/S0074-02761961000200004.» http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0074-02761961000200004&lng=en&nrm=iso

[11] GUIMARÃES, J.H. Family Tachinidae (Larvaevoridae). In: PAPAVERO, N. (ed.). A catalogue of the Diptera of the America South of the United States. São Paulo, Departamento de Zoologia, Secretaria da Agricultura, 1971, cap. 104, p 1-333. Available from: https://doi.org/10.5962%2Fbhl.title.110114>. Accessed: Oct. 8, 2016. doi: 10.5962/bhl.title.110114.
» https://doi.org/10.5962/bhl.title.110114.» https://doi.org/10.5962%2Fbhl.title.110114

[12] MATTHEWS, M. Heliothine moths of Australia. A guide to pest bollworms and related noctuid groups. Melbourne, CSIRO, 1999. Available from: <https://doi.org/10.2307/3496160 >. Accessed: Jul. 16, 2016. doi: 10.2307/3496160 .

[13] OBOPILE, M.; MOSINKIE, K.T. Integrated pest management for African bolloworm (Helicoverpa armigera) in Botswana: Review of past research and future perspectives. Journal of Food Agriculture and Environment, v.1, p.1-9, 2007. Available from: https://doi.org/10.5772%2F54522>. Accessed: Nov. 04, 2016. doi: 10.5772/54522.
» https://doi.org/10.5772/54522 » https://doi.org/10.5772%2F54522

[14] RAVLIN, F.W.; STEHR, F.W. Revision of the genus Archytas (Diptera: Tachnidae) for America North of Mexico. Miscellaneous Publications of the Entomological Society of America, v.58, p.10-38, 1984. Available from: https://doi.org/10.2307/3494472 >. Accessed: Oct. 8, 2016. doi: 10.2307/3494472.
» https://doi.org/10.2307/3494472.» https://doi.org/10.2307/3494472

[15] SANCHEZ, V.; RAVEN, C.K.G. Tachinidae (Diptera) registrados en el Museo de Entomología de la Universidad Nacional Agraria, La Molina. Revista Peruana de Entomologia, v.32, p.93-102, 1989.

[16] SHELBY KS et al. Parasitism-linked block of host plasma melanization. Journal of Invertebrate Pathology, v.75, p.218-225, 2000. Available from: https://doi.org/10.1006%2Fjipa.2000.4925>. Accessed: Jul. 02, 2016. doi: 10.1006/jipa.2000.4925.
» https://doi.org/10.1006/jipa.2000.4925.» https://doi.org/10.1006%2Fjipa.2000.4925

[17] SHEPARD, M.; STERLING, W. Incidence of parasitism of Heliothis spp. (Lepidoptera: Noctuidae) in some cotton fields of Texas. Annals of the Entomological Society of America, v.65, p.759-760 , 1972. Available from: https://doi.org/10.1093%2Faesa%2F65.3.759>. Accessed: Mar. 11, 2016. doi: 10.1093/aesa/65.3.759.
» https://doi.org/10.1093/aesa/65.3.759.» https://doi.org/10.1093%2Faesa%2F65.3.759

[18] SOSA-GÓMEZ, D.R. et al. Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Revista Brasileira de Entomologia, v. 60 , p.101-104, 2016. Available from: https://doi.org/10.1016%2Fj.rbe.2015.09.008>. Accessed: Dec. 12, 2016. doi: 10.1016/j.rbe.2015.09.008.
» https://doi.org/10.1016/j.rbe.2015.09.008.» https://doi.org/10.1016%2Fj.rbe.2015.09.008

[19] SPECHT A. et al. Morphological and molecular identification of Helicoverpa armigera (Lepidoptera: Noctuidae) and expansion of its occurrence record in Brazil. Pesquisa Agropecuária Brasileira, v.48, p. 689-692, 2013. Available from: https://doi.org/10.1590%2Fs0100-204x201300060 0015>. Accessed: Jun. 3, 2016. doi:10.1590/s0100-204x201300060 0015.
» https://doi.org/10.1590%2Fs0100-204x201300060 0015