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Ciência Rural

Print version ISSN 0103-8478On-line version ISSN 1678-4596

Cienc. Rural vol.46 no.9 Santa Maria Sept. 2016  Epub May 17, 2016 


Natural parasitism by Trichogramma spp. in agroecosystems of the Mid-North, Brazil

Parasitismo natural por Trichogramma spp. em agroecossistemas do Meio-Norte, Brasil

Ranyse Barboa Querino1  * 

Nadja Nara Pereira da Silva1 

Roberto Antonio Zucchi2 

1Embrapa Meio-Norte, 64006-220, Teresina, PI, Brasil

2Escola Superior de Agricultura "Luiz de Queiroz" (ESALQ), Universidade de São Paulo (USP), Piracicaba, SP, Brasil.


The micro-hymenopterans of genus Trichogramma are eggs parasitoids used in the biological control of lepidopteran pests. The objectives of this study was to record the interaction of species of Trichogramma and their hosts on crops in the Mid-North, in the states of Maranhão and Piauí, Brazil. Lepidopteran eggs were sampled on crops and non-crops. Trichogramma atopovirilia , T. manicobai , T. galloi and T. pretiosum occur naturally in eggs of eight lepidopteran species. Natural parasitism shown by Trichogramma species reveals the importance of these parasitoids as agents for biological control in the Mid-North region.

Key words: egg parasitoid; biological control; lepidopteran pests.


Os micro-himenópteros do gênero Trichogramma são parasitoides de ovos utilizados no controle biológico de lepidópteros. Os objetivos deste estudo foram registrar as interações de espécies de Trichogramma e seus hospedeiros em culturas agrícolas do Meio-Norte, nos estados do Maranhão e Piauí. Foram amostrados ovos de lepidópteros em culturas agrícolas e plantas não cultivadas. Trichogramma atopovirilia, T. manicobai, T. galloi e T. pretiosum ocorreram naturalmente parasitando ovos de oito espécies de lepidópteros. O parasitismo natural evidencia a importância das espécies de Trichogramma como agente de controle biológico de pragas na região do Meio-Norte.

Palavras-chave:  parasitoides de ovos; controle biológico; lepidópteros-praga.

The micro-hymenopterans of genus Trichogramma have been used in the biological control of lepidopterans pest in Brazil and other countries (PARRA & ZUCCHI, 2004). There are 26 known species of Trichogramma in Brazil, corresponding to the largest number of native species reported in a South American country (ZUCCHI et al., 2010). The species in genus Trichogramma are adapted to the climate conditions and characteristics of different habitats. This makes essential to know the existing parasitoid species of Trichogramma , their host insects and the associated plants in a given agroecosystem.

The type of agricultural system (annual crops, forest systems and fruit-growing) is another factor that must be considered when selecting the most suitable Trichogramma species to be used. For example, T. pretiosum is commonly observed in agroecosystems, whereas T. bruni is found in forest environments and on fruit trees (QUERINO & ZUCCHI, 2002, 2016).

Studies on the egg parasitoids of northern and northeastern Brazil have been largely neglected. Only five species have been reported in these regions, including three in the Northeast ( T. atopovirilia Oatman & Platner, 1983; T. galloi Zucchi, 1988; and T . pretiosum Riley, 1879) and three in the North ( T. marandobai Brun, Moraes & Soares, 1986; T. lasallei Pinto, 1999; and T. pretiosum ) (QUERINO & ZUCCHI, 2016). Trichogramma pretiosum is the only species found in both regions.

In this way, the aim of this study was to investigate the species of Trichogramma and their hosts in agroecosystems of Mid-North, Brazil. This sub-region of northeastern Brazil is located in the states of Maranhão (MA) and Piauí (PI) and has a diverse phytophysiognomy, including Cerrado, Caatinga and Mata de Cocais. The agricultural industry in Maranhão and Piauí is expanding, having occupied 2,700,000 hectares to produce over 7,000,000 metric tons of rice, cotton, corn, and soybeans in the past 15 years (CONAB, 2015).

Egg parasitoids from cultivated plants were sampled in the Mid-North of Brazil in the period from 2011 to 2013 and in 2015 (Table 1). Lepidopteran eggs were sampled from plants that were selected at random. Eggs were collected from Glycine max L. (soybean), Gossypium hirsutum L. (cotton), Manihot esculenta Crantz (cassava), Oryza sativa L. (rice), Passiflora edulis Sims. (passion fruit), Saccharum officinarum L. (sugarcane), Vigna unguiculata L. (cowpea), Zea mays L. (corn), and other, non-cultivated plants. Each egg was removed from the plant or maintained on a small piece of the leaf, which was placed in a plastic capsule and observed daily until emergence of the parasitoid or eclosion of the host larva. Parasitoids obtained were sexed and preserved in 80% ethanol, for later identification. Trichogramma males were prepared, mounted and identified using the keys according to QUERINO & ZUCCHI (2011). Voucher specimens were deposited in the Insect Collection at Embrapa Meio-Norte.

Table 1 Collection sites of Trichogramma species in the Mid-North of Brazil (Maranhão and Piauí), from 2011 to 2013 and in 2015. 

Four species of Trichogramma were obtained from lepidopteran eggs occurring naturally in agroecosystems of Mid-North Brazil: T. atopovirilia, T. manicobai , T. galloi and T. pretiosum (Table 2). This is the first report of T. manicobai in the region. With this finding, four species of Trichogramma are now known to occur in northeastern Brazil.

Table 2  Trichogramma species associated with pest lepidopterans on crops in the Mid-North of Brazil, from 2011 to 2013 and in 2015. 

*Females (identifications is not possible)

Trichogramma pretiosum was the only parasitoid species collected in all sampling sites, on eight species of Lepidoptera from five families. Trichogramma pretiosum is a generalist, infesting over 240 lepidopteran species (PINTO, 1999) and is widely distributed in Brazil (ZUCCHI et al., 2010). With the exception of Nyctelius n. nyctelius and Panoquina l. lucas (newly reported hosts), all of the other lepidopteran hosts observed in this study are economically important (Table 2).

Only T . atopovirilia and T. pretiosum were obtained from lepidopteran eggs collected on weeds and non-cultivated plants. Weeds are considered to be reservoirs of parasitoids, which can infest the eggs of pest lepidopterans in adjoining crop areas. Thus, Trichogramma pretiosum was associated to Heraclides thoas brasiliensis on Piper tuberculatum (Jacq.) ( Piperaceae ) in Teresina/PI, and to Chrysodeixis includens on Comelinna benghalensis L. ( Commelinaceae ) and Borreria sp. ( Rubiaceae ) in Bom Jesus/PI. Whereas T. atopovirilia was associated to unknown Lepidoptera species on Panicum sp. ( Poaceae ) in Teresina/PI.

Trichogramma galloi was only observed as a parasite of D . saccharalis eggs on sugarcane in Teresina, PI. Trichogramma manicobai was collected from eggs of Erinnyis ello (L., 1758) on cassava in Teresina, PI (Table 2). Both species are specialists, as T. galloi exclusively infests eggs of D. saccharalis on sugarcane and T. manicobai only infests eggs of E. ello on cassava.

The behavior of many insect groups is changing because of agricultural production systems; and therefore, their status as key pests is also changing. Among these groups, lepidopterans pest represent phytosanitary challenge. Biological control based on natural parasitism by Trichogramma is a potential strategy for managing these pests. This study makes the first report of associations between pest lepidopterans and Trichogramma spp. in the Mid-North region of Brazil. This is basic information for an effort to reveal the diversity of Trichogramma in the region, and an essential step towards conserving these parasitoids and using them in biological control programs.


To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support (No. 479343/2011-0). To Prof. Olaf Mielke for identifying the hesperiids. To Paulo Henrique Soares da Silva and José Almeida Pereira (Embrapa) for their support to our research.


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Received: September 27, 2015; Accepted: March 14, 2016; Revised: May 09, 2016

*Corresponding author: Ranyse Barboa Querino, email:

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