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Trichospilus diatraeae (Hymenoptera: Eulophidae): development and reproduction in Lepidoptera palm oil pests/Trichospilus diatraeae (Hymenoptera: Eulophidae): desenvolvimento e reproducao em lepidopteros-praga da palma de oleo.

1. Introduction

The oil palm (Elaeis guineensis Jacq.) is of African origin and the main agro-industrial activity in humid areas in the Brazilian Amazon, Colombia, Ecuador, Malaysia, Indonesia and several African countries (Hansen et al., 2015). This culture is a source of vegetable oil for food production and Bio fuels with high profitability, employment generation fixing the man in the field and reduced environmental impacts (Thawaro and Te-chato, 2010; Abdalla et al., 2008). Elaeis guineensis is well adapted to the Amazon conditions with this region being that with the largest area in the world to expansing activity (Chia et al., 2009).

The Para state is the largest palm oil producer in Brazil with an average productivity of six tonnes of oil/ha/year (Chia et al., 2009), but Lepidoptera defoliators as Opsiphanes invirae Hubner and Brassolis sophorae L. (Lepidoptera: Nymphalidae) can compromise this crop productivity (Ribeiro et al., 2010). The damage of Lepidoptera pests is incresead due to control measures deficiency without biological or synthetic chemical insecticides to be used against these pests (Ribeiro et al., 2010; Parra et al., 2009; Pereira et al., 2009a).

The natural biological control agents in palm tree crop in Brazil includes Chalcididae (Hymenoptera), Tachinidae and Sarcophagidae (Diptera) parasitizing Brassolis astyra Godart, B. sophorae, O. invirae and Opsiphanes sp. (Lepidoptera: Nymphalidae) larvae and pupae in the coconut (Cocus nucifera) (Marcicano et al., 2007, 2009) and oil palm (E. guineensis) (Tinoco et al., 2012) culture. This shows the importance of manipulating natural enemies to increase the biological control (Dobbs and Potter, 2016; Pereira et al., 2015; Smith et al., 2015).

Parasitic Hymenoptera can control insect pests, but the biology of these natural enemies in natural or alternative hosts must be understood (Boyd Junior and Held, 2016). This is necessary because the host type can affect the oviposition rate, longevity, sex ratio, body size and fecundity (Silva-Torres et al., 2009) besides life history of natural enemies (Martins et al., 2016; Valente et al., 2016).

The pupal parasitoid Trichospilus diatraeae Cherian & Margabandhu (Hymenoptera: Eulophidae) of Asian origin is gregarious, with polyphagous habit but with high prevalence in lepidopteran with its record in 1942 in the sugarcane borers, Diatraea venosata Walker (Lepidoptera: Pyralidae) (Bennett et al., 1987). This parasitoid has been studied for the biological control of pests in cucurbitaceous, eucalyptus, corn, pasture, soybean and sugar cane (Oliveira et al., 2016; Silva et al., 2015; Zache et al., 2010).

This objective was to study the biology of the parasitoid T. diatraeae in the lepidopteran oil palm B. sophorae and O. invirae.

2. Material and Methods

This work was performed at the Agropalma Plant Complex in the municipality of Tailandia, Para State, Amazon region of Brazil, 48[degrees]50'30.57" (West longitude) and 02[degrees]34'37.51" (South latitude) in a room at 25 [+ or -] 2[degrees]C, relative humidity of 70 [+ or -] 10% and photophase of 12 hours.

2.1. Rearing the alternative host

Rearing Tenebrio molitor L. (Coleoptera: Curculionidae) started with larvae obtained from the Entomology Laboratory of Embrapa Eastern Amazon, Belem, Para State. This host was kept in plastic trays (39.3 x 59.5 x 7.0 cm) in a room (25 [+ or -] 2[degrees]C, 70 [+ or -] 10% RH and 12 hours photophase) with paper sheets covering the substrate of wheat bran where these insect laid eggs. Newly hatched T. molitor were fed wheat bran (97%), yeast (3%) and chayote slices as liquid supply until the adult emergence (Zanuncio et al., 2000).

2.2. Rearing the parasitoid

Adults of T. diatraeae were kept in glass tubes (14.5 x 2.0 cm) plugged with cotton and with droplets of honey. The alternative host pupae T. molitor, up to 24 hours old, were exposed to parasitism for 48 hours at a temperature of 25 [+ or -] 2[degrees]C, relative humidity of 70 [+ or -] 10% and photophase of 12 hours followed by removal of the parasitoids (Pereira et al., 2009b).

2.3. Collecting pest species

Immature O. invirae and B. sophorae were collected in the field and transported to the laboratory of Agropalma, where they were placed in wooden cages (50 x 50 x 70 cm) and fed ad libitum with E. guineensis leaves until pupation.

2.4. Bioassay

Ten O. invirae and B. sophorae pupae weighing 1,500 [+ or -] 90 mg and 2,300 [+ or -] 200 mg, respectively, and up to 48 hours at the pupa stage were used. These pupae were individualized in glass tubes (14.5 x 2.0 cm) and exposed to parasitism by 30 T. diatraeae females, which provide high fertility and parasitoid individuals with better morphological conditions (Ribeiro et al., 2010). These females were removed from the tubes after 48 hours of exposure to the hosts. The pupae and the female parasitoid density were determined in preliminary tests. These pupae were kept in a room at 25 [+ or -] 2[degrees]C, 70 [+ or -] 10% RH and 12 h photophase until emergence of adult parasitoids or moths.

The duration of the life cycle (egg to adult), parasitism percentage, percentage and number of individuals emerged, sex ratio (number of females/total number of individuals), number of immature and parasitoid pupae that did not complete its development (host pupae were opened at forty days after parasitism and number of immature and dead parasitoid pupae counted) and the offspring longevity (males and females) were evaluated. The sex of T. diatraeae adults was determined by the morphological characteristics of the antenna and abdomen of this parasitoid (Paron, 1999).

2.5. Statistical analysis

The experiment was conducted in a randomized design with two treatments represented by the hosts (O. invirae and B. sophorae) parasitized by T. diatraeae with 10 replications, each with one host pupae. The percentage of parasitism and emergence of the progeny were subjected to nonparametric analysis of variance and when significant, compared with the Wilcoxon test at 5% significance level. The data of cycle length, parasitoid number, immature dead, sex ratio and longevity of males and females T. diatraeae per host were tested using the F 5% significance level (SAS Institute, 1997)

3. Results

Parasitism (P= 0.32) and emergency (P= 0.59) of T. diatraeae were similar in pupae of the two lepidopteran oil palm defoliator, with parasitism rates of 100% and 90% and the emergence of 60% and 50% from B. sophorae and O. invirae pupae, respectively (Figure 1).

The duration of egg-adult of T. diatraeae was shorter in O. invirae (21.50 [+ or -] 0.42 days) pupae than in those B. sophorae (27.60 [+ or -] 1.80 days) (P= 0.005) (Table 1, Figure 2). Pupae of B. sophorae (2,300 [+ or -] 200 mg) were heavier than those of O. invirae (1,500 [+ or -] 90 mg).

The numbers of adults emerged (P= 0.04) and immature mortality (P= 0.01) of T. diatraeae were higher in B. sophorae pupae (689.00 [+ or -] 89.62 and 217.13 [+ or -] 58.18) than in those of O. invirae (447.83 [+ or -] 51.52 and 13.50 [+ or -] 5.23) (Table 1). The sex ratio (P= 0.29) and the longevity (P= 0.34) of males (P= 0.29) T. diatraeae emerged from B. sophorae and O. invirae pupae were similar (Table 1).

4. Discussion

The similar parasitism of B. sophorae and O. invirae pupae by T. diatraeae confirms the generalist habit of this parasitoid, as reported with Antiearsia gemmatalis Hubner, Heliothis vireseens (Fabricius), Spodoptera frugiperda (Smith) (Noctuidae) and Diatraea saeeharalis (Fabricius) (Pyralidae) (Paron and Berti-Filho, 2000), Thyrinteina arnobia (Stoll) (Geometridae) (Pereira et al., 2008) Tenebrio molitor L. (Tenebrionidae) (Favero, 2009) and Helieoverpa armigera pupae (Lepidoptera: Noctuidae) (Oliveira et al., 2016) pupae. Moreover, the similar percentage of emergence from O. invirae and B. sophorae pupae compared to T. diatraeae confirms the quality and/or nutritional values of these host to the parasitoid, because these factors can affect the onset and development of natural enemies (Brodeur and Boivin, 2004; Zanuncio et al., 2008).

The shortest duration from egg to adult T. diatraeae in O. invirae pupae than in those of B. sophorae can be attributed to the shorter pupa stage of the host, because the faster metabolism of the host can reduce the parasitoids cycle. The solitary endoparasitoid Meteorus gyrator (Thunberg) (Hymenoptera: Braconidae) had shorter duration of the larval stage with Chrysodeixis chalates (Esper) (Lepidoptera: Noctuidae) than with four other Noctuidae species, due to increased host speed development (C. chalcites) (Smethurst et al., 2004). Moreover, competition among immature T. diatraeae in the smaller O. invirae pupae and consequently the lower food resources available compared to larger B. sophorae pupae may also resulted in the development duration in that host (Aruna and Manjunath, 2010). The longest duration of T. diatraeae development in B. sophorae pupae can reduce the chances of host survival by it increases the period vulnerable to predators, pathogens or the host response (Benrey and Denno, 1997).

The larger T. diatraeae progeny in B. sophorae pupae that in those of O. invirae demonstrates a better quality of the first host for this parasitoid reproduction, what was helped by the greater pupae (Fidgen et al., 2000; Brodeur and Boivin 2004, Silva-Torres et al., 2009). Parasitoid females usually oviposit more eggs on larger hosts known as a principle of sex allocation (Jones, 1982), by having more food for immature stages (Uckan et al., 2004). However, the immune defense of larger host can affect the development and survival of immature parasitoids (Strand and Pech, 1995; Andrade et al., 2010). The resource explored by immature T. diatraeae was similar in each host with 3.43 mg of fresh weight in B. sophorae [mean pupae weight (2,300 [+ or -] 200 mg)/average number of progeny emerged (669.0 [+ or -] 89.6)] and 3.35 mg wet weight in pupae of O. invirae [weight (1,500 [+ or -] 90 mg)/average number of progeny emerged (447.8 [+ or -] 51.5)] to produce each parasitoid adult. This confirms the hypothesis that host nutritional quality regulates the size of the population of T. diatraeae (Zaviezo and Mills, 2000; Bell et al., 2005). However, this differs from that observed for Hyssopus pallidus Askew (Hymenoptera, Eulophidae), where each milligram of wet weight of Cydia molesta Busck (lower host) produced 0.82 [+ or -] 3.8 and the same parasitoid of C. pomonella L. (Lepidoptera: Tortricidae) (bigger host) was able to produce only 0.27 [+ or -] 0.18 this parasitoid, showing nutritional quality between these different hosts (Hackermann et al., 2007).

The high number of immature dead in dissected B. sophorae pupae may be due to host immune defenses (Andrade et al., 2010) and/or the excessive egg numbers laid by T. diatraeae per host pupae (Jones, 1982). Competition among parasitoid larvae in the host can cause mortality and reduce the number of adults of these parasitoids emerged (Chong and Oetting, 2007).

A similarly high sex ratio of T. diatraeae in the lepidopteran B. sophorae and O. invirae pupae agrees with that reported for the parasitoid Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) in Bombyx mori L. (Lepidoptera: Bombycidae) pupae (Pereira et al., 2009a). This may be an Eulophidae (Pereira et al., 2010) and Ichneumonidae (Matos Neto et al., 2004) characteristic, facilitating these parasitoids to increase their populations in the laboratory and field (Matos Neto et al., 2005; Amalin et al., 2005). Furthermore, it indicates a high potential reproductive capacity of T. diatraeae for integrated management of Lepidoptera oil palm defoliators.

A similar longevity of T. diatraeae males and females emerged from B. sophorae or O. invirae pupae indicates an adequate nutritional quality of these hosts, which can affect adult parasitoids (males and females) during its immature stage (Brodeur and Boivin, 2004). The parasitoid T. diatraeae has the potential for the biological control of Lepidoptera oil palm defoliators, especially, B. sophorae.


We thank the Brazilian agencies "Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES/PELD), Fundacao de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG)," and "Programa Cooperativo sobre Protecao Florestal/ PROTEF" of the "Instituto de Pesquisas e Estudos Florestais/IPEF" for scholarships and financial support.


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R. C. Ribeiro (a) *, T. G. Pikart (b), H. A. Fouad (c), M. C. Parreira (a), J. C. Zanuncio (d), M. A. Soares (e) and V R. Castro (f)

(a) Faculdade de Agronomia, Universidade Federal do Para--UFPA, Campus Universitario do Tocantins-Cameta, CEP 68400-000, Cameta, PA, Brasil

(b) Centro de Ciencias Biologicas e da Natureza--CCBN, Universidade Federal do Acre--UFAC, CEP 69920-900, Rio Branco, AC, Brasil

(c) Faculty of Agriculture, Plant Protection Department, Sohag University, 82786, Sohag, Egypt

(d) Departamento de Entomologia--BIOAGRO, Universidade Federal de Vicosa--UFV, CEP 36570-900, Vicosa, MG, Brasil

(e) Programa de Pos-graduacao em Producao Vegetal, Universidade Federal dos Vales Jequitinhonha e Mucuri--UFVJM, CEP 39100-000, Diamantina, MG, Brasil

(f) Departamento de Engenharia Florestal, Universidade Federal de Vicosa--UFV, CEP 36570-900 Vicosa, MG, Brasil

* e-mail:

Received: December 8, 2016-Accepted: August 4, 2017-Distributed: August 31, 2019 (With 2 figures)

Caption: Figure 1. Parasitism and emergence (%) of Trichospilus diatraeae (Hymenoptera: Eulophidae) in pupae of the Opsiphanes invirae Brassolis sophorae (Lepidoptera: Nymphalidae). Means followed by the same uppercase or lowercase letter do not differ by the nonparametric of Wilcoxon test (p<0.05).

Caption: Figure 2. Accumulated percentage of Trichospilus diatraeae (Hymenoptera: Eulophidae) individuals emerged from Opsiphanes invirae and Brassolis sophorae (Lepidoptera: Nymphalidae) pupae.
Table 1. Cycle length (days), progeny, number of immature,
sex ratio, longevity (days) for males and females (mean
[+ or -] standard error) of Trichospilus diatraeae
(Hymenoptera: Eulophidae) in pupae of Lepidoptera palm oil

Biological           Opsiphanes invirae    N

Egg--adult (days)   21.50 [+ or -] 0.42b   6
Progeny             447.8 [+ or -] 51.5b   6
Number of           13.5 [+ or -] 5.23b    6
  immature dead
Sex ratio           0.95 [+ or -] 0.01a    6
Longevity of        9.95 [+ or -] 1.25a    20
  females (days)
Longevity of         9.0 [+ or -] 1.35a    10
  males (days)

Biological           Brassolis sophorae    N

Egg--adult (days)   27.60 [+ or -] 1.80a   5
Progeny             669.0 [+ or -] 89.6a   5
Number of           217.1 [+ or -] 58.2a   8
  immature dead
Sex ratio           0.97 [+ or -] 0.01a    5
Longevity of        12.0 [+ or -] 1.76a    20
  females (days)
Longevity of         7.3 [+ or -] 0.70a    10
  males (days)

Means followed by the same letter per line do not
differ by the F test (p<0.05).
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Title Annotation:Original Article
Author:Ribeiro, R.C.; Pikart, T.G.; Fouad, H.A.; Parreira, M.C.; Zanuncio, J.C.; Soares, M.A.; Castro, V.R.
Publication:Brazilian Journal of Biology
Date:May 26, 2019
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