SciELO - Scientific Electronic Library Online

vol.55 issue1Toxic effects of essential plant oils in adult Sitophilus oryzae (Linnaeus) (Coleoptera, Curculionidae)Susceptibility of Alphitobius diaperinus (Panzer) (Coleoptera, Tenebrionidae) to cypermethrin, dichlorvos and triflumuron in southern Brazil author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand



  • English (pdf)
  • Article in xml format
  • How to cite this article
  • SciELO Analytics
  • Curriculum ScienTI
  • Automatic translation


Related links


Revista Brasileira de Entomologia

Print version ISSN 0085-5626

Rev. Bras. entomol. vol.55 no.1 São Paulo Jan./Mar. 2011 



Interaction between Telenomus remus and Trichogramma pretiosum in the management of Spodoptera spp.



Maria Mirmes Paiva GoulartI; Adeney de Freitas BuenoII; Regiane Cristina Oliveira de Freitas BuenoIII; Simone Silva VieiraIV

IUniversidade de Rio Verde, 75901–970 Rio Verde-GO, Brasil.
IIEmbrapa Soja, Rodovia Carlos João Strass, s/n, Caixa postal 231, 86001–970 Londrina-PR, Brasil. Author for correspondence
IIIUniversidade de Rio Verde, 75901–970 Rio Verde-GO, Brasil.
IVCentro de Ciências Agroveterinárias, Universidade do Estado de Santa Catarina, 88520–000 Lages-SC, Brasil.




Interaction betweeen Telenomus remus and Trichogramma pretiosum in the management of Spodoptera spp. The use of egg parasitoids is a promising strategy for Integrated Pest Management (IPM), but different species of parasitoids have greater or lesser control efficiency, depending on the pest species. Recently, not only Anticarsia gemmatalis and Pseudoplusia includens but also Spodoptera cosmioides and S. eridania have been among the key Lepidoptera larvae attacking soybeans. This study evaluated the combination of Telenomus remus and Trichogramma pretiosum for parasitism of eggs of the Spodoptera complex, for better control efficiency and broader spectrum of action among the key pests of soybeans. The experiment was carried out under controlled environmental conditions (25 ± 2ºC; 70 ± 10% RH; and 14 h photophase) in a completely randomized experimental design with seven treatments and 10 replicates with S. frugiperda, S. cosmioides and S. eridania eggs. Each replicate consisted of one egg mass of each Spodoptera species, with approximately 100 eggs offered to the parasitoids. The treatments were: 1) 10 females of T. pretiosum; 2) nine females of T. pretiosum and one female of T. remus; 3) eight females of T. pretiosum and two females of T. remus; 4) seven females of T. pretiosum and three females of T. remus; 5) six females of T. pretiosum and four females of T. remus; 6) five females of T. pretiosum and five females of T. remus, and 7) 10 females of T. remus. The parameter evaluated was the percentage of parasitized eggs. Results showed that treatments combining both parasitoid species with only 1 T. remus for each 9 T. pretiosum (10%) and only 2 T. remus for each 8 T. pretiosum (20%) were enough to significantly increase the parasitism observed on eggs of S. cosmioides and S. frugiperda, respectively. This association of T. pretiosum and T. remus in different proportions is very promising for biological control in IPM programs because it provides wide spectrum of control.

Keywords: Biological control; parasitism; Scelionidae; Trichogrammatidae.


Interação de Telenomus remus e Trichogramma pretiosum no manejo de Spodoptera spp. O uso de parasitóides de ovos é uma estratégia promissora dentro do manejo integrado de pragas (MIP), mas diferentes espécies de parasitóides têm maior ou menor eficiência dependendo da espécie praga. Recentemente, não apenas Anticarsia gemmatalis e Pseudoplusia includens, mas também Spodoptera cosmioides e S. eridania estão entre as principais larvas de Lepidoptera que estão atacando a cultura da soja. Assim, este trabalho avaliou a possibilidade do uso associado de Telenomus remus e Trichogramma pretiosum no controle de ovos do complexo Spodoptera, objetivando uma maior eficiência de parasitismo com um maior espectro de ação entre as pragas-chave desta cultura. O experimento foi conduzido em condições controladas (25 ± 2ºC; 70 ± 10% e fotofase de 14 h) no delineamento inteiramente casualizado com 7 tratamentos e 10 repetições e ovos de S. frugiperda, S. cosmioides e S. eridania. Para cada repetição foi oferecida aos parasitóides uma postura de cada uma das espécies de Spodoptera, com aproximadamente 100 ovos. As diferentes proporções dos parasitóides (tratamentos) avaliadas foram: 1) dez fêmeas de T. pretiosum 2) nove fêmeas de T. pretiosum e uma fêmea de T. remus 3) oito fêmeas de T. pretiosum e duas fêmeas de T. remus 4) sete fêmeas de T. pretiosum e três fêmeas de T. remus 5) seis fêmeas de T. pretiosum e quatro fêmeas de T. remus 6) cinco fêmeas de T. pretiosum e cinco fêmeas de T. remus 7) dez fêmeas de T. remus. O parâmetro avaliado foi à porcentagem de ovos parasitados. Os resultados mostraram que tratamentos combinando ambas as espécies de parasitóides com apenas 1 T. remus para cada 9 T. pretiosum (10%) e apenas 2 T. remus para cada 8 T. pretiosum (20%) foram suficientes para aumentar significativamente o parasitismo observado em ovos de S. cosmioides e S. frugiperda, respectivamente. Esta associação de T. pretiosum e T. remus em diferentes proporções é bastante promissora para utilização em programas de controle biológico dentro do MIP visto que poderá fornecer um bom espectro de controle.

Palavras-chave: Controle biológico; parasitismo; Scelionidae; Trichogrammatidae.



Soybean is one of the most important export products of Brazil, and in the crop season 2008/2009 57.1 million tons were produced in the country (CONAB 2009). Currently, in the main Brazilian production regions, besides the key pest of this crop, the velvetbean caterpillar, Anticarsia gemmatalis Hübner, 1818 (Lepidoptera, Noctuidae), other species of Lepidoptera have caused extensive damage on soybean crops. Among them are other Noctuidae, such as the soybean-looper, Pseudoplusia includens Walker, 1857 and some species of the genus Spodoptera, as the southern armyworm, Spodoptera eridania Cramer, Spodoptera cosmioides Walker (Bueno et al. 2007) and the fall armyworm, Spodoptera frugiperda J. E. Smith, 1797.

In order to maximize agricultural production, pest control should have an interdisciplinary and multidisciplinary vision, integrating different control methods that are less harmful to humans and to the environment. In this context, the adoption of additional tactics for the successful control of insect pests can be incorporated within the IPM philosophy. Among those control tactics, parasitoid releases have shown good results, particularly for the management of insect pests of the order Lepidoptera (Parra 2006). The egg parasitoids of the genus Trichogramma (Hymenoptera, Trichogrammatidae) have been among the most studied and used species. The use of parasitoids have several advantages, such as easy rearing on alternative hosts and massive releases for the control of key pests of several crops such as cotton, sugar cane, vegetables, corn, soybean, tomato, and also stored grains (Parra & Zucchi 2004).

Despite the generalist feeding habits, the parasitoids of the genus Trichogramma are typically less efficient in controlling species of Spodoptera. This is more evident in species that oviposit in overlapping layers, since these parasitoids are able to parasitize only the upper layers of the egg masses. In this context, an efficient egg parasitoid is Telenomus remus Nixon (Hymenoptera, Scelionidae), because it is notable for parasitizing even those eggs located in the inner layers of the egg masses (Cruz & Figueiredo 1994). Thus, T. remus can be considered as one of the species with the greatest potential for the biological control of Spodoptera spp. (Johnson 1984). However, there is a barrier to the use of T. remus on large scale release, because it cannot be reared on alternative hosts. This important fact would increase costs, since the rearing of Spodoptera is more costly and complex than rearing alternative hosts used for Trichogramma spp. Thus, the association of T. remus with T. pretiosum may be a good option for the management of the Spodoptera complex. Therefore, the objective of this study was to evaluate the association of T. remus and T. pretiosum to control larvae of the Spodoptera complex.



This research was carried out in laboratory in controlled environmental conditions of 25 ± 2ºC temperature, 70 ± 10% relative humidity, and 14 h photophase. It was used a completely randomized experimental design, with seven treatments and 10 replicates using S. frugiperda, S. cosmioides and S. eridania eggs. The insects for the experiments were from laboratory rearing, and the adults of T. pretiosum and T. remus were multiplied on eggs of Anagasta kuehniella Zeller, 1879 (Lepidoptera, Pyralidae) and S. frugiperda, respectively.

Previously defined proportions of T. remus and T. pretiosum females were placed into 10 cm high x 2 cm in diameter glass vials, containing a droplet of honey for the parasitoids to feed on. The S. frugiperda, S. eridania and S. cosmioides egg masses, with about 100 eggs each, were glued to 4 cm x 1.5 cm white cardboard and introduced in the tubes containing the different proportions of each parasitoid. The treatments were: 1) 10 females of T. pretiosum; 2) nine females of T. pretiosum and one female of T. remus; 3) eight females of T. pretiosum and two females of T. remus; 4) seven females of T. pretiosum and three females of T. remus; 5) six females of T. pretiosum and four females of T. remus; 6) five females of T. pretiosum and five females of T. remus; and 7) 10 females of T. remus.

After 24 h of parasitism, the cardboard pads with the parasitized eggs were removed from the vials and placed into transparent plastic bags, until the emergence of the adult parasitoids. The parameter evaluated was the percentage of parasitized eggs. Results were submitted to exploratory analysis to evaluate the assumptions of normality of residues, homogeneity of variance of treatments and additivity of the model to allow for ANOVA implementation. The means were then compared by the Tukey test at 5% probability.



The treatments with 2 T. remus for each 8 T. pretiosum (20%) or higher proportion of T. remus presented the most effective parasitism of S. frugiperda eggs compared to the other treatments. The lowest percent parasitism was observed in the treatment where only T. pretiosum females were present (Fig. 1A). The greater efficiency in the treatments with T. remus is because this parasitoid is able to parasitize the eggs of the inner layers, affecting the entire egg mass (Fernandes & Carneiro 2006). On the other hand, this characteristic of Spodoptera spp. – oviposition in overlapping layers – provides a limitation to the parasitism by Trichogrammatidae. The impact of the number of S. frugiperda egg layers on the parasitism of Trichogramma atopovirilia Oatman & Platner has been previously reported in the literature, when the parasitism detected in single layer egg masses was higher than that observed in egg masses with two and three egg layers (Beserra & Parra 2005).



Differently, the usual limitation to the parasitism by Trichogrammatidae regarding to parasitism on Spodoptera spp. do not occur for T. remus. It is important to emphasize that the parasitism capacity of T. remus on eggs of S. frugiperda is considerably high (Bueno et al. 2008; Bueno et al. 2010). Each T. remus female produces about 270 offspring during their reproductive lifespan (Morales et al. 2000) and performs the oviposition of one egg per host, thus superparasitism is unusual in this species (Cave 2000). However, the superparasitism on eggs parasitized by Trichogramma spp. is not a rare event. In assessing parasitism and superparasitism of T. pretiosum on eggs of Sitotroga cerealella Olivier 1819 (Lepidoptera, Gelechiidae) a lower reproductive success of that parasitoid was observed (Moreira et al. 2009).

The same increment in efficiency observed for eggs of S. frugiperda, in relation to percentage of parasitism, was also observed for eggs of S. cosmioides, when T. remus was added to the treatments (Fig. 1B). That occurred because the arrangement of the S. cosmioides egg mass is similar to that of S. frugiperda, both being arranged in overlapping layers, hindering the action of T. pretiosum.

In contrast, for the parasitism of S. eridania eggs there was no statistical difference among the treatments with and without T. remus. It was found that even in the treatment with T. pretiosum alone, the parasitism was higher than 70% (Fig. 1C). It should be emphasized that the S. eridania eggs are not laid in overlapping layers, thus T. pretiosum can parasitize almost all eggs of the egg mass. This explains the good performance of parasitism with the release of only T. pretiosum females, which did not occur when the hosts were S. frugiperda and S. cosmioides eggs.

The choice of the parasitoid to be released for controlling the Spodoptera complex on soybeans is very important, mainly because this complex of species has grown in importance in recent crop seasons (Bueno et al. 2009). Among the natural enemies of Spodoptera spp., the egg parasitoid T. remus stands out as the most common species of the genus, being already found parasitizing five different species of Spodoptera spp. (Morales et al. 2000). This parasitoid has been used in large-scale IPM programs in Venezuela, released in areas of corn, reaching rates of parasitism up to 90% on eggs of S. frugiperda (Ferrer 2001). If from one standpoint T. remus proved to be very efficient in the management of the Spodoptera complex, from another it is important to consider that on soybean crops, other caterpillars of economic importance also occur in association with Spodoptera spp, such as larvae of P. includens (Bueno et al. 2007). Therefore, the use of T. remus associated with T. pretiosum proves to be a good option in the biological control of soybean caterpillars. T. pretiosum was reported as the best species to be used against P. includens (Bueno et al. 2009). These larvae infest the crops during the reproductive stage and in addition to defoliation; they feed and damage the pods. During this period, the plant has a well-developed foliar architecture, thus impairing chemical control, which has often been ineffective due to the large amount of leaves that the plants have at that stage (Bueno et al. 2007).

Unlike the chemical control, the use of egg parasitoids can be more efficient because the parasitoid can search for the pest, even in a well developed soybean plant. In this case, the choice of the parasitoid species is of utmost importance. T. pretiosum has the advantage of being generalist, controlling several insect pests of the order Lepidoptera that attack soybean, such as P. includens (Bueno et al. 2009) and A. gemmatalis (Zachrisson & Parra 1998). Furthermore, the large-scale rearing of this parasitoid has lower production cost and is easier to carry out as compared to the multiplication of T. remus. However, T. pretiosum has the great disadvantage of not being efficient on pests that lay their eggs in overlapping, layers such as S. cosmioides and S. frugiperda. Despite being more efficient on these insect pests, T. remus is a parasitoid specific to the genus Spodoptera and would not have a good performance against other moths of economical importance on soybean crops, as P. includens, which occurs in the same period as Spodoptera spp. Thus, the combination of both is a good strategy for Lepidoptera control in soybean crops.



The parasitoid T. pretiosum, when released solely for parasitizing eggs of S. frugiperda and S. cosmioides, under controlled environmental conditions, is less efficient than when released associated with the parasitoid T. remus. Treatments combining both parasitoid species with only 1 T. remus for each 9 T. pretiosum (10%) and only 2 T. remus for each 8 T. pretiosum (20%) were sufficient to significantly increase the parasitism up to rates statistically equivalent to the treatment with 100% of T. remus observed in eggs of S. frugiperda and S. cosmioides, respectively, under controlled laboratory conditions. For the biological control of S. eridania, the parasitoids T. remus and T. pretiosum, when released alone or in combination, under laboratory conditions, do not show statistically significant differences on percentage of parasitism. Experiments in the field should be carried out in the future to ratify these laboratory results for field conditions.



Thanks are expressed to Embrapa Soja, CNPq and CAPES for the financial support, making this research possible. This paper was approved for publication by the Editorial Board of Embrapa Soja as manuscript number 01/2010.



Beserra, E. B. & L. R. P. Parra. 2005. Impacto do número de camadas de ovos de Spodoptera frugiperda no parasitismo por Trichogramma atopovirilia. Scientia Agricola 62: 190–193.         [ Links ]

Bueno, R. C. O. F; J. R. P. Parra; A. F. Bueno; F. Moscardi; J. R. G. Oliveira & M. F. Camillo. 2007. Sem barreira. Revista Cultivar 93: 12–15.         [ Links ]

Bueno, R. C. O. F.; T. R. Carneiro; D. Pratissoli; A. F. Bueno & O. A. Fernandes. 2008. Biology and thermal requirments of Telenomus remus reared on fall armyworm Spodoptera frugiperda eggs. Ciência Rural 38: 1–6.         [ Links ]

Bueno, R. C. O. F.; J. R. P. Parra; A. F. Bueno & M. L. Haddad. 2009. Desempenho de tricogramatídeos como potenciais agentes de controle de Pseudoplusia includens Walker (Lepidoptera: Noctuidae). Neotropical Entomology 38: 389–394.         [ Links ]

Bueno, R. C. O. F.; T. R. Carneiro; A. F. Bueno; D. Pratissoli, O. A. Fernandes & S. S. Vieira. 2010. Parasitism capacity of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) eggs. Brazilian Archives of Biology and Technology 53: 133–139.         [ Links ]

Cave, R. D. 2000. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News and Information 21: 21–26.         [ Links ]

CONAB – COMPANHIA NACIONAL DE ABASTECIMENTO. 2009. Available from: (accessed 22 July 2009).         [ Links ]

Cruz, I. & M. L. C. Figueiredo. 1994. Estudos preliminares do parasitóide Telenomus sp. Nixon sobre ovos de Spodoptera frugiperda 1992/1993: Relatório técnico anual do Centro Nacional de Pesquisa de Milho e Sorgo 6: 104–105.         [ Links ]

Fernandes, O. A. & T. R. Carneiro. 2006. Controle biológico de Spodoptera frugiperda no Brasil, p. 75–82. In: A. S. Pinto; D. E. Nava; M. M. Rossi & D. T. Malerbo-Souza (ed.). Controle biológico de pragas na prática. Piracicaba, CP 2, 287 p.         [ Links ]

Ferrer, F. 2001. Biological control of agricultural insect pest in Venezuela; advances, achievements, and future perspectives. Biocontrol News and Information 22: 67–74.         [ Links ]

Johnson, N. F. 1984. Systematics of Nearctic Telenomus: classification and revisions of the Podisi and Phymatae species groups (Hymenoptera: Scelionidae) Knull. Columbus, Ohio State University, 113 p.         [ Links ]

Morales, J.; J. S. Gallardo; C. Vásquez & Y. Rios. 2000. Patrón de emergência, longevidad, parasitismo y proporción sexual de Telenomus remus (Hymenoptera: Scelionidae) com relación al cogollero del maíz. Bioagro 12: 47–54.         [ Links ]

Moreira, M. D.; M. C. F. Santos; E. B. Beserra; J. B. Torres & R. P. Almeida. 2009. Parasitismo e superparasitismo de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) em ovos de Sitotroga cerealella (Oliver) (Lepidoptera: Gelechiidae). Neotropical Entomology 38: 237–242.         [ Links ]

Parra, J. R. P. 2006. A prática do controle biológico de pragas no Brasil. p. 11–24. In: A. S. Pinto; D. E. Nava; M. M. Rossi & D. T. Malerbo-Souza (ed.). Controle biológico de pragas na prática. Piracicaba, ESALQ/USP, 287 p.         [ Links ]

Parra, J. R. P. & R. A. Zucchi. 2004. Trichogramma in Brazil: feasibility of use after twenty years of research. Neotropical Entomology 33: 271–281.         [ Links ]

Zachrisson, B. A. & J. R. P. Parra. 1998. Capacidade de dispersão de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) para o controle de Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae) em soja. Scientia Agricola 55: 133–137.         [ Links ]



Received 5/1/2010;
accepted 13/1/2011



Editor: Sonia Maria Noemberg Lázzari

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License