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Chilean journal of agricultural research

On-line version ISSN 0718-5839

Chilean J. Agric. Res. vol.73 no.2 Chillán June 2013 


Biological characteristics of Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) on refrigerated pupae of Anticarsia gemmatalis Hubner (Lepidoptera: Noctuidae)


Fabricio Fagundes Pereira1, José Cola Zanuncio2, Samir Oliveira Kassab1*, Patrik Luiz Pastori3, Rogério Hidalgo Barbosa1, and Camila Rossoni1

1Universidade Federal da Grande Dourados, Faculdade de Ciencias Biológicas e Ambientais, 79.804-970, Dourados, Mato Grosso do Sul, Brasil. "Corresponding author (
2Universidade Federal de Viçosa, Departamento de Biologia Animal, 36570-000, Viçosa, Minas Gerais, Brasil.
3Universidade Federal do Ceará, Departamento de Fitotecnia, Campus Universitário do Pici, 60.356-000, Fortaleza, Ceará, Brasil.

Mass rearing of parasitoids is a fundamental step for biological control programs. The biological characteristics of Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) were evaluated in pupae of Anticarsia gemmatalis Hubner (Lepidoptera: Noctuidae) stored at low temperatures. Twenty four hours-old pupae of A. gemmatalis were stored at 12 °C for 0, 1, 3, 6, 9, and 12 d and then exposed to parasitism by P. elaeisis females. The life span of P. elaeisis was affected and ranged from 19 to 24 d on the pupae of the host. Parasitism reached 100% of the host pupae after storage in all periods at 12 °C, and adults emerged from 20.00 to 54.54% of them. The progeny of P. elaeisis ranged from 71 to 198 and had an inverse relationship with the increase in the storage period. Pupae of A. gemmatalis may be stored for up to 6 d at 12 °C and subsequently used in rearing of P. elaeisis.

Key words: Biological control, parasitism, parasitoid rearing, temperature.



Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) is a parasitoid with potential for use in the control of Lepidoptera of economic importance (Pereira et al., 2010), which has been reported in insects of the families Arctiidae (Zaché et al., 2012a), Bombycidae (Pereira et al., 2009), Crambidae (Bittencourt and Berti-Filho, 2004; Chichera et al., 2012), Noctuidae (Bittencourt and Berti-Filho, 1999; 2004; Andrade et al., 2010), and Lymantriidae (Zaché et al., 2012b).

The use of parasitoids depends on selection of a suitable host for mass rearing (Bittencourt and Berti-Filho, 1999; Paron and Berti-Filho, 2000; Pereira et al., 2010; Pastori et al., 2012). Large-scale rearing of parasitoids is fundamental for the implementation of biological control programs and the lack of artificial diets requires the use of a large number of preferred hosts or alternatives for production (Pratissoli et al., 2003; Milward-de-Azevedo et al., 2004).

Natural enemies maybe reared on alternative hosts with low production cost and that do not reduce their efficiency of control on the natural host (Pratissolli et al., 2005; Zanuncio et al., 2008). Anticarsia gemmatalis Hubner, 1818 (Lepidoptera: Noctuidae) has a short life cycle, it can be reared on artificial diet, and the pupae are hosts for development of P. elaeisis (Bittencourt and Berti-Filho, 1999; 2004; Andrade et al., 2010; Pereira et al., 2010). However, the conservation of this host at low temperatures has not yet been studied and for this reason the present study was developed. In order to investigate the reproductive capacity of parasitoids on pupae stored at low temperatures, it is important to synchronize both parasitoid and host demands while seeking mass production of these natural enemies for release in the field (Pereira et al., 2009).

The objective of this study was to evaluate the biological characteristics of P. elaeisis on A. gemmatalis pupae stored at 12 °C for different periods of time.


Experiments were performed at the laboratory of Controle Biológico de Insetos in Departamento de Biologia Animal of Universidade Federal de Viçosa (UFV), Viçosa, Minas Gerais, Brazil, with the following steps:

Rearing of insects
Rearing of A. gemmatalis was initiated with eggs from the rearing stock, maintained on artificial diet in the laboratory of Controle Biológico de Insetos in Departamento de Biologia Animal of Universidade Federal de Viçosa. These eggs were placed on moistened filter paper in 10.0 cm diameter x 2.5 cm height Petri dishes. Newly-hatched larvae were transferred with a fine brush to plastic containers containing artificial diet. The plastic containers with newly-hatched larvae were maintained in a room at 25 ± 2 °C, 70 ± 10% relative humidity (RH) and 12:12 h photoperiod until transformation into pupae.

Pupae of A. gemmatalis were placed in 20 x 20 x 20 cm creen cages, lined on the sides with bond paper as substrate for oviposition, and the emerging adults were fed with a 10% honey in water of the plastic containers (3.0 cm in diameter x 4.0 cm in height), through an inserted cotton wick, a methodology adapted from Greene et al. (1976).

Rearing of adults of P. elaeisis were kept in jars labeled 12.5 cm diameter x 17.0 cm height, closed with fine cloth and contained plastic containers (3.0 cm diameter x 4.0 cm height) and parasitoids feeding with droplets of honey. Pupae of A. gemmatalis or Thyrinteina arnobia (Stoll, 1972) (Lepidoptera: Geometridae) aging 24 to 72 h were exposed to parasitism for 24 h at a temperature of 25 ± 2 °C, 70 ± 10% RH, and 12:12 h photoperiod, a methodology adapted from Pereira et al. (2010).

Experimental design
Twenty four hours-old pupae of A. gemmatalis were weighed 0.196 ± 3.61 g (reducing the effects of host biomass variation) and stored at 12 °C (temperature base) as proposed by Magrini et al. (1996). The host pupae were stored by 1, 3, 6, 9, or 12 d and in the control host pupae of the same age were used, but without storage at 12 °C. Each pupa was exposed to parasitism by six females of 72 h-old P. elaeisis in 14 cm x 2.2 cm glass tubes plugged with cotton, for 24 h at 25 ± 2 °C, 70 ± 10% RH, and 12:12 h photoperiod, after which, they were removed from the tubes. The egg to adult period life cycle duration parasitism percentage [discounting natural mortality (Abbott, 1925)], emergence percentage of the progeny, number of parasitoids emerged per host pupa, offspring longevity and sex ratio were determined. Parasitoids were sexed by morphology of their antennae and abdomens (Delvare and LaSalle, 1993).

The treatments were 0, 1, 3, 6, 9 or 12 d storage periods. Ten replicates were used in a completely randomized design, where each replicate was a pupa of A. gemmatalis. The data on life cycle duration, progeny of P. elaeisis emerged per pupa of A. gemmatalis, sex ratio and longevity of female parasitoids were subjected to ANOVA at 5% probability and regression analysis. Selection of the equation that best fit to the data was performed using polynomial models, based on the coefficient of determination (R2), the significance of the regression coefficients (Pi) and regression testing by the F-test (up to 5% probability).

Data of parasitism percentage and emergence of P. elaeisis were subjected to analysis of generalized linear models with binomial distribution (P < 0.05) using the R Statistical System (Ihaka and Gentleman, 1996). This analysis was performed with the original non-parametric data, but data a represented in percentage to facilitate viewing.


Palmistichus elaeisis parasitized 100% of A. gemmatalis pupae, with adult emerging from 20 to 54.54% of the host pupae subjected to the different storage periods at 12 °C, respectively (x2 = 6.977, P = 0.008) (Figure 1).

Figure 1. Percentage of Anticarsia gemmatalis pupae (Lepidoptera: Noctuidae) with emergence of Palmistichus elaeisis (Hymenoptera: Eulophidae) after storage for 0, 1, 3, 6, 9, or 12 d at 12 °C, 70 ± 10% RH, and 12:12 h photoperiod (X = 6.977; P = 0.008).

The duration of the pre-reproductive period (egg to adult) of P. elaeisis on pupae of A. gemmatalis after storage for 0 to 12 d at 12 °C was affected and ranged from 19 to 24 d, respectively (R2Treat = 0.4279; F = 6.1489; P = 0.0202; df = 26) (Figure 2).

Figure 2. Duration of egg to adult (days) of Palmistichus elaeisis (Hymenoptera: Eulophidae) on pupae of Anticarsia gemmatalis (Lepidoptera: Noctuidae) after storage for 0, 1, 3, 6, 9, or 12 d at 12 °C, 70 ± 10% RH, and 12:12 h photoperiod. (F = 6.1489, P = 0.0202).

Progeny of P. elaeisis per pupae of A. gemmatalis ranged 71 to 198 and presented an inverse relationship with the increase in storage period (R2Treat = 0.8017; F = 7.3937; P = 0.0117; df = 26) (Figure 3). The sex ratio of P. elaeisis was similar for the 0 to 12 d storage periods of A. gemmatalis pupae at 12 °C, with means of 0.94 to 0.95 (P > 0.05), respectively.

Figure 3. Progeny ofPalmistichus elaeisis (Hymenoptera: Eulophidae) per pupa of Anticarsia gemmatalis (Lepidoptera: Noctuidae) after storage for 0, 1, 3, 6, 9, or 12 d at 12 °C, 70 ± 10% RH, and 12:12 h photoperiod (F = 7.3937, P = 0.0117).


Longevity of P. elaeisis females emerged from pupae of A. gemmatalis decreased with the increase in storage period of these pupae at 12 °C (R2Treat = 0.4641; F = 10.8649; P = 0.0014; df = 89) (Figure 4).

Figure 4. Longevity of Palmistichus elaeisis females (Hymenoptera: Eulophidae) on emerged pupae of Anticarsia gemmatalis (Lepidoptera: Noctuidae) after storage for 0, 1, 3, 6, 9, or 12 d at 12 °C, 70 ± 10% RH, and 12:12 h photoperiod (F = 10.8649, P = 0.0014).


Palmistichus elaeisis developed on pupae of A. gemmatalis after being stored at 12 °C for different periods of time. The similarity in duration of the life cycle of P. elaeisis on pupae of A. gemmatalis not refrigerated or stored for up to 6 d at 12 °C indicates that host pupae at these conditions are suitable for the development of this parasitoid.

Pupae can maintain physiological and/or suitable nutritional conditions for parasitoids a certain period, but this varies with the host species and/or parasitoid (Pereira et al., 2009; 2010; Pastori et al., 2012). Muscidifurax uniraptor Kogan & Legner (Hymenoptera: Pteromalidae) had a lower reproductive capacity on pupae of Musca domestica (Linnaues, 1758) (Diptera: Muscidae) after storage for 1 to 2 d when compared to those not refrigerated. However, reproduction of M. uniraptor on M. domestica pupae stored for a longer period of time was greater than or similar to the control (Thomazini and Berti-Filho, 2000), as observed herein for P. elaeisis in pupae of A. gemmatalis.

Insect pupae possess an immune response against immature parasites, but are not able to maintain this defense mechanism (encapsulation rate and toxin production) active for a long time due to high metabolic costs (Schmidt et al., 2001; Schmid-Hempel, 2005; Andrade et al., 2010). The increased period of development of P. elaeisis on pupae of A. gemmatalis after storage at 12 °C for 9 to 12 d may be due to inadequate quality for the development of the juvenile parasitoid. This is due to the fact that refrigeration for long periods can injure the cells of pupae, which compromises their sequence of metabolic reactions and therefore its nutritional quality (Milward-de-Azevedo et al., 2004; Pereira et al., 2009).

The high rates of parasitism and emergence of P. elaeisis on A. gemmatalis pupae after storage at 12 °C, mainly until the sixth day, confirm that the conservation of hosts at low temperatures is useful for parasitoid production programs (Pratissoli et al., 2003; Milward-de-Azevedo et al., 2004; Pratissoli et al., 2005; Zanuncio et al., 2008).

Palmistichus elaeisis produced progeny on pupae of A. gemmatalis after storage at 12 °C during all time periods. However, there was a trend for a decreased reproductive capacity of P. elaeisis with an increase in the storage period at 12 °C. The smaller progeny of this parasitoid on A. gemmatalis pupae after 9 and 12 d of storage at 12 °C may be related to morphological and physiological changes, even a reduced metabolism (Chapman, 1998; Pereira et al., 2009; Andrade et al., 2010). The effects of these morphological and physiological changes in the progeny of parasitoids are unknown, but it may be possible to determine the degree of susceptibility to the development of these natural enemies (Pfannenstiel et al., 1996).

The sex ratio of P. elaeisis was greater than 93%, which is important in mass rearing systems, laboratory experiments and selection of individuals for release in the field. The predominance of females over males can increase the number of individuals produced in the next generation and can positively contribute to the control of agricultural pests after field releases (Uckan and Gulel, 2002; Amalin et al., 2005).

The longevity of P. elaeisis females that emerged from pupae of A. gemmatalis presented a decrease when increasing the storage period of these pupae at 12 °C. Nevertheless, females of P. elaeisis lived long enough to ensure their reproduction, as the pre-oviposition and oviposition periods of this parasite in pupae of A. gemmatalis are 1.00 ± 0.75 and 16.6 ± 0.75 d, respectively (Bittencourt and Berti-Filho, 1999). This is important because in mass rearing of parasitoids, survivability is one of the requirements for insect control (Van-Lenteren, 2000).

The use of parasitoids for biological control programs depends on development and reproductive success of the natural enemy on pupae of the preferred and/or alternative host with suitable nutritional conditions and low production cost. Palmistichus elaeisis develops on pupae of A. gemmatalis stored at 12 °C and this is important for programmed rearing in the lab in order to synchronize the emergence of the parasitoid with the presence of the stage of development of the target host, as well as appropriating the mass rearing efficiency and program for release of P. elaeisis.


Pupae of Anticarsia gemmatalis stored at 12 °C for up to 6 d were suitable for rearing of Palmistichus elaeisis since they favored a greater progeny, with minor variations between the percentage of progeny, emergence and egg to adult duration.


We thank the Brazilian institutions "Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenagao de Aperfeigoamento de Pessoal de Nível Superior (CAPES) and Fundagao de Amparo à Pesquisa do estado de Minas Gerais (FAPEMIG)".


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Received: 29November 2012. Accepted: 29 March 2013.

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