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1 December 2015 Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) in the Pupae of Diaphania hyalinata (Lepidoptera: Crambidae) of Various Ages
Isabel Moreira Da Silva, Teresinha Vinha Zanuncio, Fabricio Fagundes Pereira, Carlos Frederico Wilcken, José Eduardo Serrão, José Cola Zanuncio
Author Affiliations +

Trichospilus diatraeae Cherian & Margabandhu (Hymenoptera: Eulophidae) is a gregarious parasitoid of a wide variety of lepidopterans including melonworm, Diaphania hyalinata L. (Lepidoptera: Crambidae), pupae in the field. The latter is a key pest of Cucurbitaceae; it primarily damages their leaves and secondarily their fruit, and it reduces the productivity of the plants. The aim of this study was to determine the effect of the age of D. hyalinata pupae on the development of T. diatraeae. Diaphania hyalinata pupae aged 24, 48, 72, 96, 120, and 144 h were individualized and exposed to eight 48-h-old T. diatraeae females for 24 h. The emergence and parasitism rates, sex ratios, and longevities of T. diatraeae males and females were found to be similar with D. hyalinata pupae of different ages. The number of progeny, width of the head capsule, and duration of the life cycle (egg to adult) of T. diatraeae decreased with the increasing age of D. hyalinata pupae. Importantly, the number of parasitoid progeny per host pupa and size of the parasitoid adults were larger when 24-h-old host pupae were parasitized than when 48- to 144-h-old pupae were parasitized. Trichospilus diatraeae was very effective in parasitizing D. hyalinata pupae of ages ranging from 24 to 144 h.

Cucurbitaceae (Cucurbitales) such as Citrullus lanatus (Thunb.) Matsumara & Nakai , Cucurbita maxima Duchesne, Cucurbita moschata Duchesne, and Cucurbita pepo L. are rich in substances that help preventing diseases (Achu et al. 2005). Pests can reduce the productivity of plants of this family throughout the vegetative and reproductive stages (Gonring et al. 2003; Dhillon et al. 2005; Santana et al. 2012). Diaphania species are widely distributed in America, and they feed on Cucurbitaceae leaves, twigs, and shoots (Surís et al. 1997; Gonring et al. 2003; Melo et al. 2011).

Parasitoids are important in the context of their diversity and the parasitism levels they inflict on the host populations (Olivera & Bordat 1996; Pikart et al. 2011; Tavares et al. 2012). Eulophidae (Hymenoptera), the largest family of Chalcidoidea with 4,472 species in 297 genera, occur in temperate and tropical areas and are ectoparasitoids (Eulophinae and Euderinae) or endoparasitoids (Entedoninae and Tetrastichinae) of insects of different orders (Pereira et al. 2008; Zanuncio et al. 2008; Talebi et al. 2011; Zaché et al. 2011). The use of parasitoids in biological control programs may depend on the availability of a host species with suitable characteristics for the development and maturation of these natural enemies (Lemos et al. 2003; Pastori et al. 2012; Tavares et al. 2012). The generalist habit of Trichospilus diatraeae Cherian & Margabandhu (Hymenoptera: Eulophidae) renders this parasitoid as a promising agent for biological control (Ribeiro et al. 2013; Rodrigues et al. 2013). Trichospilus diatraeae parasitized Diaphania hyalinata L. (Lepidoptera: Crambidae) pupae in the field at a level that showed a considerable potential for its use in the biological control of this pest (Melo et al. 2011). Trichogramma species (Hymenoptera: Trichogrammatidae) and Tachinidae species have been reported to parasitize D. hyalinata eggs and larvae, respectively (Gonring et al. 2003; Polanczyk et al. 2011).

The quality of the host used to mass rear parasitoids for biological control can affect the reproduction and parasitism capacity of these natural enemies (Tran & Takasu 2000; Pereira et al. 2009). Koinobiont parasitoid species parasitize young or early-stage hosts in which they can proceed through their development, and they usually do not kill the host until the parasitoid reaches its final developmental stage (Kant et al. 2012). In contrast, idiobiont parasitoid species, such as T. diatraeae, usually parasitize an immobile stage of the host, i.e., egg or pupa— but some also parasitize larvae —, and prevent its further development. The age and quality of the host pupa at the time of parasitism can affect the quality of the progeny of the idiobiont (Imandeh 2006).

Parasitoids depend on the host as a single resource for their offspring, and the host age determines its nutritional quality, which can affect the progeny of the parasitoids (Husni & Honda 2001; Imandeh 2006; Caron et al. 2010). The host age can affect sex ratio, progeny size (Hansan et al. 2009; Pereira et al. 2009), life cycle (Husni & Honda 2001), and longevity (Imandeh 2006) of parasitoids. Furthermore, the hormonal and cellular host defenses against parasitism depend on the host's developmental stage (Hegazi & Khafagi 2008). Trichospilus diatraeae has been reported to parasitize D. hyalinata, wherefore the aim of this study was to evaluate the parasitism and development of this parasitoid in this host's pupae of different ages.

Materials and Methods

The study was conducted at the Laboratory of Biological Control of Insects (LCB) of the Institute of Biotechnology Applied to Agriculture (BIOAGRO) of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil.


Diaphania hyalinata larvae were kept in plastic pots (3 L) each of which had a spout, and sealed with organza. The larvae were fed daily with chayote (Sechium edule [Jacq.] Sw.; Cucurbitales: Cucurbitaceae) leaves from the 1st instar to pre-pupa stage. Then, they were placed in plastic containers lined with paper towels for pupation. For adult emergence, the pupae were transferred to closed wooden cages with screened sides. Adult Lepidoptera received a cotton wad soaked with a nutrient solution composed of honey and water (1:1) at the bottom of the cage on a Petri dish. Pumpkin leaves were placed inside the cages as oviposition site, and egg masses were collected and placed in plastic pots.

Trichospilus diatraeae adults were kept in glass tubes (14.0 × 2.2 cm) containing drops of honey as food and plugged with cotton. Pupae of the alternative host Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae) were obtained from the rearing facility of the LCB/Dep. de Biologia Animal (DBA)/UFV, and these pupae were exposed individually to parasitism by 10 T. diatraeae females for 24 h for rearing of this parasitoid (Pereira et al. 2009).


Twelve D. hyalinata pupae (100-120 mg) per age (24, 48, 72, 96, 120, and 144 h) were individualized and exposed for 24 h to eight 72 hold T. diatraeae females. These pupae were isolated in glass tubes (2.2 × 14.0 cm) capped with cotton in a room at 25 ± 0.2 °C, 70 ± 10.8% RH, and a 12:12 h L:D photoperiod until the emergence of either parasitoid adults or host adults (Pereira et al. 2009).

We evaluated the duration of the life cycle (egg to adult), the percentage of parasitism and emergence, the number of parasitoids emerged, sex ratio (SR = the number of females/number of adults), width of the head capsule, and longevity of T. diatraeae males and females. Sex was determined by morphological characteristics of the antenna and abdomen of these parasitoids (Paron 1999), and the size of the head capsule and body was measured with an ocular micrometer attached to a stereomicroscope. The longevity and the size of the head capsule of T. diatraeae were evaluated in 20 females and 15 males.

The completely randomized design experiments were conducted with 12 D. hyalinata pupae per treatment. Data were subjected to analysis of variance (ANOVA) at the 5% level, and when significant, they were subjected to regression analysis. Parasitism and emergence rates of T. diatraeae from D. hyalinata pupae were subjected to ANOVA and the non-parametric Kruskal-Wallis test (SAS Institute 1997).


The age of D. hyalinata pupae when first parasitized did not affect percentage of parasitism and percentage of emergence of T. diatraeae, because the rate of parasitism was 100% in all treatments (Fig. 1), and the rate of emergence from 72-, 96-, and 120-h-old pupae was 83.33% and that from 24-, 48-, and 144-h-old pupae was 91.67% (Fig. 1). The number of T. diatraeae offspring per pupa declined with increasing age of the D. hyalinata pupae, and the largest number of progeny was obtained from 24-h-old pupae (F = 138.036, P = 0.0003, R2 = 0.9718) (Fig. 2A). The duration of the lifecycle of T. diatraeae (egg to adult) peaked in 48- to 72-h-old pupae and then decreased with the increasing age of the D. hyalinata pupae (F = 49.9171, P = 0.0197, R2 = 0.9520) (Fig. 2B). The widths of the head capsule of females (F = 49.9171, P = 0.0197, R2 = 0.8241) and males (F = 13.9139, P = 0.0203, R2 = 0.7767) T. diatraeae decreased with the increasing age of the D. hyalinata pupae (Figs. 2C and 2D, respectively), but the longevities of males and females of this parasitoid did not vary significantly with the age of the host pupa (Table 1). The sex ratios (proportions of females) of T. diatraeae adult progeny that emerged from D. hyalinata pupae that had been parasitized at ages ranging from 24 h to 144 h were similar and varied between 0.91 and 0.94 (Table 1).

Fig. 1.

Percentage of parasitism of Diaphania hyalinata pupae and percentage of emergence of Trichospilus diatraeae progeny from D. hyalinata hosts parasitized as 24-, 48-, 72-, 96-, 120-, and 144-h-old pupae. Bars with the same uppercase or lowercase letter do not differ by the non-parametric Kruskal-Wallis test (P > 0.05).


Fig. 2.

Trichospilus diatraeae progeny produced in Diaphania hyalinata pupae; (A) number of progeny; (B) duration of the T. diatraeae life cycle; (C) width of the T. diatraeae female head capsule; (D) width of the T. diatraeae male head capsule (mean ± SE). Measurements were made on T. diatraeae that emerged from D. hyalinata hosts parasitized as 24-, 48-, 72-, 96-, 120-, and 144-h-old pupae.



Because the age of D. hyalinata pupae when first parasitized did not affect percentage of parasitism and percentage of emergence of T. diatraeae, young pupae (24 h) can be used to reduce the rearing costs. The independence of these important life parameters from the age of host pupae should help the parasitoid to maintain its populations in the field.

The percentages of parasitism and emergence of T. diatraeae from D. hyalinata pupae of different ages differ from those observed for Diadromus collaris (Gravenhorst) (Hymenoptera: Ichneumonidae) from Plutella xylostella L. (Lepidoptera: Plutellidae) pupae (Wang & Liu 2002). The parasitism capacity of D. collaris decreased with increasing age of its host due to selection and preference for younger pupae that present better nutrition quality for the development of its progeny (Wang & Liu 2002; Pizzol et al. 2012). In comparison, despite the possible decline in the nutritional quality of D. hyalinata, T. diatraea showed greater flexibility during oviposition. The age of the host can reduce its suitability due to the hardening of its puparium, which hinders the penetration of the ovipositor, but female parasitoids can change the oviposition place on the pupa (King 2011).

The reduction of the number of progeny of T. diatraeae that emerged from older D. hyalinata pupae may be due to decreased food quality resulting from the conversion of hemolymph into adult tissues (Minot & Leonard 1976; Pereira et al. 2009). The presence of dead T. diatraeae individuals inside 144-h-old D. hyalinata pupae showed that this parasitoid had oviposited in this host at this age. The diminished production of offspring per host pupa in 144-h-old pupae indicated that pupae of advanced age were less suitable for the development of immature parasitoids, probably due to morphological and physiological changes, which can influence the acceptability and suitability of hosts by parasitoids (Wang & Liu 2002), as was reported for the reduction in number of progeny of Nesolynx thymus (Girault) and Palmistichus elaeisis Delware & LaSalle (Hymenoptera: Eulophidae) with the increasing age of pupae of Exorista sorbillans (Wiedemann) (Diptera: Tachinidae) and Bombyx mori L. (Lepidoptera: Bombycidae), respectively (Hansan et al. 2009; Pereira et al. 2009). Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae) eggs aged more than 4 d were not parasitized by Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae), suggesting reduced suitability of S. cerealella eggs with their increasing age (Fatima et al. 2009).

Table 1.

Mean ± SE longevity of females and males in days and sex ratio of Trichospilus diatraeae that emerged from Diaphania hyalinata hosts parasitized as 24-, 48-, 72-, 96-, 120-, and 144-h-old pupae.


Gregarious endoparasitoids depend on host nutrients for their embryonic development (Haeckermann et al. 2007). Females of T. diatraeae may have laid similar numbers of eggs, regardless of the host pupa age, but a smaller number of immatures may have completed the life cycle in older hosts likely due the diminished food quality (increasing competition) (Wylie 1963; Husni & Honda 2001). Alternatively, the parasitoid females may have laid fewer eggs in older hosts with poor physiological suitability for the development of their larvae (Pizzol et al. 2012). The latter occurs when female parasitoids have oviposition strategies to maximize reproductive fitness, including survival of their immature progeny (Hegazi & Khafagi 2008). However, the use of older pupae by parasitoid species may be advantageous for their survival when host density is sparse (Husni & Honda 2001).

The shorter time of development of T. diatraeae with the increasing age of the D. hyalinata pupae differs from that of Brachymeria lasus (Walker) (Hymenoptera: Chalcididae) and Melittobia acasta (Walker) (Hymenoptera: Eulophidae), which had life cycle durations independent of the increasing age of the host (Husni & Honda 2001; Imandeh 2006). However, when Trichogramma cacaeciae Marchal (Hymenoptera: Trichogrammatidae) females parasitized older Lobesia botrana Denis & Schiffermüller (Lepidoptera: Tortricidae) eggs, their progeny had a shorter development period than that developing in younger host eggs (Pizzol et al. 2012). These reports show that parasitoids differ in their capacities to utilize resources from hosts of different ages (Tran & Takasu 2000).

The similar sex ratios of T. diatraeae from D. hyalinata pupae of diverse ages suggests that the older host did not affect the parasitoid progeny sex ratio and that high numbers of fertilized eggs were laid regardless of this parameter (Husni & Honda 2001). By contrast, the parasitoid N. thymus had lower proportions of females with older (Hansan et al. 2009) or super-parasitized hosts (Nieuwenhove & Ovruski 2011). This shows the ability in some species of female parasitoids to regulate the offspring sex ratio in response to the host and environmental conditions (Chow & Mackauer1996; Caron et al. 2010; Nieuwenhove & Ovruski 2011). The similar survival of T. diatraeae offspring with differing ages of D. hyalinata pupae again showed that the parasitoid could adapt to this condition with the development of its immatures, as observed for Gronotoma micromorpha (Perkins) (Hymenoptera: Figitidae) (Abe 2009).

The smallest width of the head capsule of T. diatraeae individuals emerging from the oldest D. hyalinata pupae indicated that the advanced development of this host, especially with 144-h-old pupae, reduced the food available to the parasitoid offspring (also effecting a shorter life cycle) and thus resulted in smaller individuals of this natural enemy. Similarly, the parasitoid B. lasus had smaller individuals in older hosts, which may indicate inadequate or reduced food availability (Husni & Honda 2001).

In conclusion, D. hyalinata pupae of various ages were parasitized by T. diatraeae, but the number of parasitoid progeny per host pupa and the size of the parasitoid adults were larger when 24-h-old host pupae were parasitized than when 48- to 144-h-old pupae were parasitized.


We thank “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq),” “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES),” and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” for financial support. Global Edico Services revised and proofread the English of the submitted version this manuscript.

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Isabel Moreira Da Silva, Teresinha Vinha Zanuncio, Fabricio Fagundes Pereira, Carlos Frederico Wilcken, José Eduardo Serrão, and José Cola Zanuncio "Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) in the Pupae of Diaphania hyalinata (Lepidoptera: Crambidae) of Various Ages," Florida Entomologist 98(4), 1025-1029, (1 December 2015).
Published: 1 December 2015
host pupa age
host quality
idade da pupa
qualidade do hospedeiro
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