First report of Dolichozele koebelei Viereck , 1911 ( Hymenoptera : Braconidae ) on larvae of Spodoptera frugiperda ( J . E . Smith , 1797 ) ( Lepidoptera : Noctuidae ) in maize ( Zea mays L . ) under different cropping systems

In the context of the modern agriculture, pest control is important in order to increase productivity in maize (Zea mays L.). However, this control should be done rationally, prioritising environmentally safer methods such as biological control. This paper aims to report the occurrence of Dolichozele koebelei Viereck, 1911 (Hymenoptera: Braconidae) in Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) larvae collected in maize subjected to different cropping systems. The experiment was conducted at the Centro Nacional de Pesquisa de Milho e Sorgo (CNPMS) in Sete Lagoas, Minas Gerais State, Brazil, using organic and conventional production. Ten plants were sampled from each of the 24 plots and for each production system, three times a week during the entire cycle of maize (variety BR 106). In the laboratory, larvae were distributed in individual rearing containers with artificial diet until the end of the biological cycle. An increased number of S. frugiperda larvae was observed in organic single crop maize; hence a higher percentage of S. frugiperda larvae parasitised by Hymenoptera and Diptera also occurred in the maize under this production system. Dolichozele koebelei had not yet been described in association with larvae of S. frugiperda. The percentage of parasitism of S. frugiperda larvae was high in both experiments, indicating the importance of natural control agents in reducing the population density of S. frugiperda, and especially the importance of an appropriate crop management.


Introduction
Maize (Zea mays L.) is one of the most important crops in Brazil, presenting record production and productivity.Nevertheless, there is still scope for increase.The production is mainly used in the animal production segment (feed and silage) and obtained in almost all Brazilian States, with lower expression in the North (Cruz et al., 2011).
Many pests are important in the maize agroecosystem, and are well known especially in conventional cultivation.The production of maize in the organic system still needs greater research effort to determine the exact occurrence and economic importance of each pest species (Macfadyen et al., 2009;Bengtsson et al., 2005).The fall armyworm, Spodoptera frugiperda (J.E. Smith, 1797) (Lepidoptera: Noctuidae), is especially important among these pests, and can reduce the production of grains in 15-73% under favourable conditions (Cruz andTurpin, 1982, 1983;Cruz et al., 1996Cruz et al., , 1999;;Hruska and Gould, 1997;Figueiredo et al., 2006a, b), with losses estimated at over 400 million dollars (Cruz et al., 1999).
In the context of modern agriculture, pest control is important to achieve higher productivity in maize.However, this control should be done rationally, aiming for the reduction in the use of pesticides and must prioritise other environmentally safer methods such as biological control, which enables the reduction in contamination of the producer, product, consumer and environment.This method can be lower in cost, and the wealth of the Brazilian fauna can be used to act as potential agents of pest control (Silva et al., 2011).
Knowledge of species and the flow of natural biological control agents in agricultural areas are essential to establish integrated management programmes.Among the insects of interest for use in biological control of S. frugiperda, parasitoids, due to their efficiency and specificity in relation to the host, have been considered the most important.
The subfamily Macrocentrinae Foerster (Hymenoptera: Braconidae) has about 150 described species; they can be solitary or gregarious, the gregarious species being polyembryonic.Most members of this subfamily have long legs and are koinobiont endoparasitoids of Lepidoptera larvae of the families: Gelechiidae, Noctuidae, Oecophoridae, Pyralidae, Tineidae, Tortricidae and Sesiidae (Achterberg, 1993).
The aim of this study was to report the occurrence of Dolichozele koebelei Viereck, 1911 (Hymenoptera: Braconidae; Macrocentrinae) in larvae of S. frugiperda collected in maize under different cropping systems.

Material and Methods
The experiments were conducted during the 2010/2011 season in the Cerrado region, in field trials and in the Laboratório de Criação de Insetos (Lacri) of the Centro Nacional de Pesquisa de Milho e Sorgo (CNPMS), in Sete Lagoas, Minas Gerais State, Brazil (19 ° 28' S and 44 ° 15' W).

Experiment I (conventional x organic maize)
This experiment was implemented on December 15, 2010.Two areas of approximately one hectare were cultivated in organic and conventional systems.The areas were isolated from one another by distances greater than 3,000 metres and both were under maize (BR 106) cultivation in the tillage system.

Experiment II (organic single crop maize x organic maize intercropped with beans)
This experiment was sown in May 23, 2011 in the area used for organic farming, divided in two areas of approximately one hectare, isolated from other areas of cultivation for about 3,000 metres.Maize (BR 106) was cultivated in one of them; in the other, maize and bean (Phaseolus vulgaris L., BRS Radiante) were sown in the same line, using the conventional tillage system.
In order to determine the initial occurrence and frequency of moths during each experiment, a delta trap (Ferocon 1C  ) containing the synthetic sex pheromone of S. frugiperda (BIO SPODOPTERA  -Chem Tica Internacional, S.A.) sachet was installed in the centre of each experimental area soon after the emergence of maize plants (Cruz et al., 2010(Cruz et al., , 2012)).
Each planting area was divided into 24 plots of equal size, and 20 samples were collected when the presence of S. frugiperda was detected in the traps.Ten plants at random per plot were collected, three times a week throughout the entire crop cycle, totalling 240 plants per sampling.
The plants were evaluated in the Lacri (acclimatised room at 25 ± 2 °C, RH 70 ± 10% and photoperiod of 12 hours), separating the larvae by species and placing them individually in plastic cups containing artificial diet (Cruz, 2009) where they remained until the end of the cycle.The pest stage in which each parasitoid emerged was annotated.
The parameters evaluated were: total number of larvae of S. frugiperda, the average number of larvae per sample; percentage of larvae parasitised by Hymenoptera or Diptera and participation of D. koebelei in the percentage of parasitised larvae.

Results
In Experiment I, 1124 larvae of S. frugiperda (Figures 1a-b) were collected in the conventional maize, being 56.2 the average number of larva per sample and 4.7% of the larvae was parasitised by Hymenoptera or Diptera.The participation of D. koebelei in the total number of parasitised larvae was 9.8%.In organic maize, 1112 larvae of S. frugiperda were collected, with an average number of 46.3 larvae per sample and 5.7% of the total number of larvae were parasitised by Hymenoptera or Diptera.The participation of D. koebelei in the total number of parasitised larvae was 11.1%.
In Experiment II (organic maize intercropped with beans) 1401 larvae of S. frugiperda were collected, with the average number of 70.0 larvae per sample.Considering the total number of larvae, 16.7% were parasitised by Hymenoptera or Diptera.The participation of D. koebelei in the total number of parasitised larvae was 1.9%.In organic single maize, 1602 larvae of S. frugiperda were collected, with an average of 80.1 larvae per sample.Among the total number of larvae collected, 19.9% were parasitised by Hymenoptera or Diptera.The participation of D. koebelei in the total number of parasitised larvae was 1.2%.
The specimens of D. koebelei were identified by one of the authors of this work (A.M.P.D.) and are deposited in the Coleção Entomológica do Departamento de Ecologia e Biologia Evolutiva -DCBU, Universidade Federal de São Carlos -UFSCar in São Carlos, São Paulo State, Brazil, and in Lacri.

Discussion
Dolichozele koebelei (Figures 1c-f) has not been described in association with larvae of S. frugiperda.The presence of D. koebelei in conventional and organic maize, shows the potential of this parasitoid as a biological control agent for use in natural integrated pest management in this culture.
Many parasitoids are associated with S. frugiperda; some exclusively parasitise eggs, such as the idiobionts

Figure 1 .
Figure 1.a) and b).Larvae of S. frugiperda; c) and d) Pupa and male adult of D. koebelei; e) and f).Pupa and female adult of D. koebelei.