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1 December 2016 Foraging Activity of Palmistichus elaeisis (Hymenoptera: Eulophidae) at Various Densities on Pupae of the Eucalyptus Defoliator Thyrinteina arnobia (Lepidoptera: Geometridae)
Rogério Hidalgo Barbosa, José Cola Zanuncio, Fabricio Fagundes Pereira, Samir Oliveira Kassab, Camila Rossoni
Author Affiliations +

Parasitoids are the main component of biological control of Lepidoptera defoliators in forested areas, and the densities of host insects can affect the efficiency of these natural enemies. The aim of this work was to study the biology and parasitism of Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) at various densities of females on individual pupae of Thyrinteina arnobia Stoll (Lepidoptera: Geometridae), the major Lepidoptera pest in eucalyptus (Myrtaceae) plantations in Brazil. Thyrinteina arnobia pupae were exposed to P. elaeisis females at various parasitoidto-host ratios: (1:1, 3:1, 6:1, 9:1, 12:1, 15:1, 18:1, and 21:1), with 12 replications. The parasitism (81.8%) and emergence (100%) rates of P. elaeisis on T. arnobia pupae were highest with 15 ovipositing females per host. The life cycle (egg to adult) of P. elaeisis was shortest (19.8 ± 0.5 d) at a ratio of 21:1. The largest production of P. elaeisis per T. arnobia pupa was obtained at the ratios of 15:1 (298.4 ± 5.0) and 18:1 (287.4 ± 4.3). The female sex ratio of parasitoid offspring was highest (0.97 ± 0.01) with a parasitoid-to-host ratio of 12:1. The density of 15 P. elaeisis females per T. arnobia pupa was the most appropriate one for providing high parasitism (81.8%), emergence (100%), and progeny (298.4 ± 5.0) of this parasitoid.

Parasitoids are important natural enemies for the equilibrium of agroecosystems because they have high species and hosts diversity (Oliveira et al. 2000; Pratissoli et al. 2005). Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) parasitizes and develops in Lepidoptera pupae of the families Arctiidae (Pereira et al. 2008), Bombycidae (Pereira et al. 2010), Crambidae (Bittencourt & Berti-Filho 2004; Chichera et al. 2012), Lymantriidae (Tavares et al. 2011; Zaché et al. 2012), Muscidae (Zaché et al. 2013), Noctuidae (Bittencourt & Berti-Filho 2004; Andrade et al. 2010; Pereira et al. 2013), Nymphalidae (Tavares et al. 2013a), Notodontidae (Zanuncio et al. 2015), Papilionidae (Tavares et al. 2013b), and Saturniidae (Pereira et al. 2008); it also develops in Coleoptera pupae of the family Tenebrionidae (Zanuncio et al. 2008). Furthermore, this parasitoid was recorded in pupae of Thyrinteina arnobia Stoll and Thyrinteina leucoceraea Rindge (Lepidoptera: Geometridae), which characterizes it as a potential biological control agent in Eucalyptus (Myrtaceae) plantations (Pereira et al. 2008, 2011).

Thyrinteina arnobia is the major lepidopteran pest in eucalypt plantations with outbreaks in several regions of Brazil (Oliveira et al. 2005) and causes significant yield losses (Bragança et al. 1998). This pest has been controlled with insecticides that have the potential to cause mortality of natural enemies and contaminate the environment (Oliveira et al. 2011). Hence, there is need to develop lower-impact control methods for this pest (Pereira et al. 2008).

Natural enemies can reduce outbreaks of defoliator Lepidoptera in eucalypt plantations (Zanuncio et al. 1993; Zanuncio et al. 1998; Guedes et al. 2000; Zanetti et al. 2003), and the use of P. elaeisis in biological control programs depends on the development of mass rearing methods for this natural enemy (Pereira et al. 2011; Menezes et al. 2012). The density of female parasitoids per host can affect parasitism (Sampaio et al. 2001), progeny sex ratio (Chong & Oetting 2006, 2007), life cycle length, and the longevity of the offspring (Pereira et al. 2010).

Palmistichus elaeisis is a gregarious parasitoid, and the optimal proportion of its females per host pupa can increase efficiency and production of this natural enemy. The aim of this work was to study the biology and parasitism of P. elaeisis in T. arnobia pupae with various densities of females of this parasitoid.

Materials and Methods

The experiment was conducted at the Laboratory of Biological Control of Insects of the Animal Biology Department/Instituto de Biotecnologia Aplicada á Agropecuária (BIOAGRO) of the Universidade Federal de Viçosa (UFV) in Viçosa, Minas Gerais, Brazil.


Rearing of the Host

Eggs of T. arnobia were obtained from the laboratory rearing stock of the Laboratory of Biological Control of Insects of the UFV. Larvae, soon after hatching, were placed in organza cloth bags (0.70 × 0.40 cm) containing eucalypt branches (from 6-mo-old plants of Eucalyptus cloeziana F. Muell.) and provided with fresh branches every 3 d, until they reached the pupal stage. Pupae were removed from these bags, sexed, separated in couples, and placed in plastic pots (500 mL) with a hole in the center of the plastic lid sealed with an organza mesh screen. Paper strips were fixed to the inside of the lids for oviposition, and pots were kept in a room at 25 ± 2 °C, 70 ± 10% RH, and a 14:10 h L:D photoperiod (adapted from Oliveira et al. 2010).

Rearing of the Parasitoid

Adults of P. elaeisis were kept in glass tubes (14 cm height × 2.5 cm diameter) sealed with cotton and containing a drop of honey to feed the parasitoids. Bombyx mori L. (Lepidoptera: Bombycidae) pupae (obtained from the company Fiação de Seda Bratac S/A, Brazil), 48 to 72 h old, were exposed to parasitism by P. elaeisis for 24 h at 25 ± 2 °C, 70 ± 10% RH, and a 12:12 h L:D photoperiod to maintain a colony of the parasitoid (Pereira et al. 2008).


Thyrinteina arnobia pupae that were 24 to 48 h old were individually exposed to 72- to 96-h-old P. elaeisis females (Andrade et al. 2012) in glass tubes (14 cm height × 2.5 cm diameter) and placed in a chamber maintained at 25 ± 2 °C, 70 ± 10% RH, and a 12:12 h L:D photoperiod, at density treatments of 1, 3, 6, 9, 12, 15, 18, and 21 parasitoids per host. After 48 h, the P. elaeisis females were removed from the tubes. The duration of the life cycle (egg to adult), percentage of parasitism [(number of pupae of T. arnobia with emergence of parasitoid + pupae without adult emergence of T. arnobia) ÷ (total number of pupae) × 100] (discounting the natural mortality of the host) (Abbott 1925), emergence [(number of pupae of T. arnobia with adult emergence of parasitoids)÷(number of parasitized pupae) × 100], progeny (adults of P. elaeisis emerged per T. arnobia pupa), body length (mm), width of the head capsule (mm) (size measurements were performed with an ocular micrometer attached to a stereomicroscope), and sex ratio (number of females per number of adults) were obtained. The sex of adult parasitoids was determined by the morphological characteristics of their antennae and abdomen. Compared with males, females are usually larger in size, have a larger abdomen, and have no pigmentation between the thorax and abdomen (LaSalle 1994). The treatments were set up with 12 replications in a completely randomized design.


The data on duration of life cycle and the number of parasitoids emerged per T. arnobia pupa were subjected to analysis of variance and, when significant at 5% probability, to a regression analysis. The parasitism and emergence rates of P. elaeisis were subjected to a binomial distribution analysis (P ≤ 0.05). The data of sex ratio, body length (mm), and width of the head capsule (mm) of P. elaeisis females and males were subjected to analysis of variance and, when significant at 5% probability, to the Scott-Knott test.


The percentage of parasitism was influenced by the densities of P. elaeisis per T. arnobia pupa and ranged from 58.3 to 81.8% (Fig. 1). The percentage of parasitoid emergence was 28.6, 42.9, 62.5, 75.0, 87.5, 100, 89.9, and 50.0% at the densities of 1, 3, 6, 9, 12, 15, 18, and 21 parasitoids per host, respectively (Fig. 1).

The duration of the life cycle (egg to adult) decreased with increasing density of P. elaeisis females from 25 to 18 d (ŷ = 24.518 − 1.0024x + 0.09066327x2 − 0.00254969x3; F = 14.2446; P = 0.0001; R2 = 0.7102) (Fig. 2A). The density of P. elaeisis females per T. arnobia pupa influenced the progeny of this parasitoid (ŷ = 133.217 + 140.043 / (1 + exp (−(x − 13.8951) / 0.0248825)); F = 4.1382; P = 0.0117; R2 = 0.85), with a minimum of 30 and a maximum of 724 P. elaeisis offspring produced at the densities of 1 and 15 parasitoids per host pupa, respectively (Fig. 2B). The sex ratio of P. elaeisis emerged from T. arnobia pupae ranged from 0.46 ± 0.45 to 0.97 ± 0.01 (number of females per total number of adults) without differences between the densities of 3 to 21 parasitoids per host (P > 0.05) (Table 1).

Fig. 1.

Percentage of pupae parasitized and percentage of emergence of Palmistichus elaeisis with a density of 1, 3, 6, 9, 12, 15, 18, or 21 ovipositing females per Thyrinteina arnobia pupa at 25 ± 2 °C, 70 ± 10% RH, and a 12:12 h L:D photoperiod. Statistical significance: parasitism, P = 0.3770; emergence, P = 0.034.


Fig. 2.

(A) Duration of life cycle (egg to adult) and (B) numbers of Palmistichus elaeisis progeny with a density of 1, 3, 6, 9, 12, 15, 18, or 21 ovipositing females per Thyrinteina arnobia pupa at 25 ± 2 °C, 70 ± 10% RH, and a 12:12 h L:D photoperiod.


Table 1.

Sex ratio (number of females / [number of females + males]), body size, and width of the head capsule of Palmistichus elaeisis (mean ± standard error) progeny emerged with a density of 1, 3, 6, 9, 12, 15, 18, or 21 ovipositing females per Thyrinteina arnobia pupa at 25 ± 2 °C, 70 ± 10% RH, and a 12:12 h L:D photoperiod.


The body length (mm) of emerged P. elaeisis females ranged from 2.02 ± 0.01 to 2.28 ± 0.02 and that of males from 1.71 ± 0.02 to 1.78 ± 0.01, with no differences between the different densities of this parasitoid (P > 0.05) (Table 1). The width of the head capsule (mm) of emerged P. elaeisis females did not differ between treatments (P > 0.05), whereas that of males ranged from 0.47 ± 0.01 to 0.51 ± 0.01, with differences between treatments (P ≤ 0.05).


The density of P. elaeisis females per T. arnobia pupa affected the percentage of parasitism, percentage of emergence, and viability of the offspring of this parasitoid. Thyrinteina arnobia pupae may have effective defense mechanisms against P. elaeisis because the emergence of these parasitoids was low at the densities of 1 and 3 parasitoids per host. Another hypothesis is that the size of this host requires a larger number of parasitoids to neutralize its immune system (Smilanich et al. 2009; Pereira et al. 2010; Altoé et al. 2012; Hood et al. 2012).

The reproduction of P. elaeisis was different from that of the parasitoid Trichospilus diatraeae Cherian & Margabandhu (Hymenoptera: Eulophidae) in pupae of Anticarsia gemmatalis Hübner, Heliothis virescens (F.), Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), Diatraea saccharalis (F.) (Lepidoptera: Crambidae), and Tenebrio molitor L. (Coleoptera: Tenebrionidae) exposed to one or more females of this parasitoid (Paron & Berti-Filho 2000; Favero et al. 2013). The variability in reproductive success may be related to inadequate proportions of female parasitoids per host, which reduced oviposition and toxin injections necessary to reduce the immune response of the host (Andrade et al. 2010; Cusumano et al. 2010; Harvey et al. 2013). In contrast, the parasitism and emergence ratios of P. elaeisis from B. mori pupae were similar with different densities of this parasitoid, suggesting that B. mori did not present nutritional or physiological barriers for the development of P. elaeisis (Pereira et al. 2010).

The short life cycle (egg to adult) of P. elaeisis in T. arnobia pupae can be explained by competition among parasitoid larvae and by physical or physiological suppression by the host, as reported for this parasitoid in B. mori pupae (Pereira et al., 2010). This pattern has also been reported with different densities of T. diatraeae in pupae of T. molitor (Favero et al. 2013) and D. saccharalis (Rodrigues et al. 2013). Besides the parasitoid density, the host species can affect the development period of parasitoids. This effect can be attributed to differences in nutritional quality and size of pupae, because the host is the food source and shelter for immatures of these natural enemies and, if inappropriate, impedes their development (Pastori et al. 2012).

The greatest number of P. elaeisis individuals produced per T. arnobia pupa at the densities of 15 and 18 parasitoids per host shows that 15 females of this natural enemy are sufficient to counteract defense mechanisms of this host. On the other hand, densities of 1, 3, 6, 9, and 21 females per T. arnobia pupa reduced the number of progeny of this parasitoid. This finding indicates that inadequate proportions of females per host result in reduced oviposition or increased competition and death of immature parasitoids (Pereira et al. 2010). The density of the parasitoid females per host pupa can reduce fertility and efficiency of mass rearing, primarily due to mortality of immatures within the pupae (Harvey et al. 2013) and competition between adults during oviposition (Pereira et al. 2013).

The high sex ratio (i.e., the predominance of females) of P. elaeisis offspring in T. arnobia pupae is important because parasitoid females are responsible for the parasitism and progeny production (Rodrigues et al. 2013) as reported for this parasitoid with A. gemmatalis, B. mori, and D. saccharalis pupae (Pereira et al. 2010, 2013; Chichera et al. 2012). Moreover, the sex ratio of P. elaeisis in T. arnobia pupae was higher than in Sarsina violascens (Herrich-Schaeffer) (Lepidoptera: Lymantriidae), likely due to differences in nutritional value, physiological barriers, and defense capacity of S. violascens pupae (Zaché et al. 2012). A decrease in sex ratio as a function of host species may reduce the efficacy of P. elaeisis parasitism, because parasitism is maximized when a large number of females is produced (Pereira et al. 2010).

The size range of P. elaeisis adults with different densities of parasitoid females can be explained by the limited resources of the host pupa as the number of larvae developing inside the host increases (Tian et al. 2008; Harvey et al. 2013). A reduced body size may reduce the efficiency of biological control, because body size is positively correlated with indicators of quality of parasitoids such as longevity, fecundity, progeny emerged, and sex ratio (Pereira et al. 2010).

The parasitism and development of P. elaeisis, independent of the density of its females, on T. arnobia pupae demonstrate that this natural enemy has potential to reduce outbreaks and possible damage caused by this insect defoliator in eucalyptus plantations. Successful rearing of this parasitoid will depend on the density of ovipositing females per host pupa.


We thank the Brazilian institutions Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Apoio à Pesquisa de Ensino e a Cultura de Mato Grosso do Sul (FAPEMS) for financial support.

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Rogério Hidalgo Barbosa, José Cola Zanuncio, Fabricio Fagundes Pereira, Samir Oliveira Kassab, and Camila Rossoni "Foraging Activity of Palmistichus elaeisis (Hymenoptera: Eulophidae) at Various Densities on Pupae of the Eucalyptus Defoliator Thyrinteina arnobia (Lepidoptera: Geometridae)," Florida Entomologist 99(4), 686-690, (1 December 2016).
Published: 1 December 2016

biological control
controle biológico
lagarta do eucalipto
looper of eucalyptus
parasitoide de pupa
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