The density of females of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) affects their reproductive performance on pupae of Bombyx mori L. (Lepidoptera: Bombycidae)

BIOLOGICAL SCIENCES

The density of females of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) affects their reproductive performance on pupae of Bombyx mori L. (Lepidoptera: Bombycidae)

Fabricio F. Pereira^I; José C. Zanuncio^II; José E. Serrão^III; Teresinha V. Zanuncio^II; Dirceu Pratissoli^IV; Patrik L. Pastori^V

^IFaculdade de Ciências Biológicas e Ambientais, Universidade Federal da Grande Dourados, Rodovia Dourados/Itahum, km 12, 79804-970 Dourados, MS, Brasil

^IIDepartamento de Biologia Animal, Universidade Federal de Viçosa, Av. PH Rolfs s/n Campus Universitário, 36570-000 Viçosa, MG, Brasil

^IIIDepartamento de Biologia Geral, Universidade Federal de Viçosa, Av. PH Rolfs s/n Campus Universitário, 36570-000 Viçosa, MG, Brasil

^IVDepartamento de Produção Vegetal, Centro de Ciências Agrárias, Universidade Federal do Espírito Santo, Alto Universitário s/n, Caixa Postal 16, 29500-000 Alegre, ES, Brasil

^VDepartamento de Fitotecnia (Pós-graduação), Universidade Federal de Viçosa, Av. PH Rolfs s/n Campus Universitário, 36570-000 Viçosa, MG, Brasil

^{Correspondence to}

ABSTRACT

Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) is a gregarious and polyphagous parasitoid mainly of Lepidoptera pupae. The objective of this paper as to study the developent of parasitoid on Bombyx mori L. (Lepidoptera: Bombycidae) pupae exposed to one, nine, 18, 27, 36, 45 or 54 female P. elaeisis, respectively. The females of the parasitoid remained in contact with pupae for 24 hours in glass tubes (14.0 x 2.2 cm), packed in a climatic chamber regulated at 25 ± 2°C, 70 ± 10% relative humidity and photo phase of 12 hours. With the exception of density 1:1 (72.72%), in other densities parasitism was 100%. Adults of P. elaeisis did not emerge from pupae at densities of 1:1 and 9:1, but 100.0% of parasitoid emergence was observed at the density of 45:1 and 54.54% at 54:1. The duration of the life cycle of this parasitoid ranged from 20 to 28 days. P. elaeisis produced 49 to 589 descendants per pupa of B. mori. The sex ratio of P. elaeisis ranged from 0.93 ± 0.01 to 0.97 ± 0.01 without differences with 18, 27, 36, 45 and 54 females/host. This parasitoid should be reared with the density of 45 females per pupa of B. mori.

Key words: alternative host, biological control, mass rearing, parasitism rate, parasitoids.

RESUMO

Palmistichus elaeisis Delvare e LaSalle (Hymenoptera: Eulophidae) é um parasitóide polífago, que inviabiliza, principalmente, pupas de lepidópteros. O objetivo desse trabalho foi estudar o desenvolvimento do parasitóide em pupas de Bobyx mori L. (Lepidoptera: Bombycidae) expostas a uma, nove, 18, 27, 36, 45 ou 54 fêmeas de P. elaeisis, respectivamente. As fêmeas do parasitóide permaneceram em contato com as pupas por 24 horas em tubos de vidro (14,0 x 2,2 cm), acondicionadas em câmara climatizada regulada a 25 ± 2°C, 70 ± 10% de UR e fotofase de 12 horas. Com exceção da densidade 1:1 (72,72%), nas demais densidades o parasitismo foi 100%. Adultos de P. elaeisis não emergiram nas densidades de 1:1 e 9:1, mas observou-se 100% de emergência do parasitóide na densidade 45:1 e 54,54% em 54:1. A duração do ciclo de vida desse parasitóide variou de 20 a 28 dias. P. elaeisis produziu de 49 a 589 descendentes por pupa de B. mori. A razão sexual de P. elaeisis variou de 0,93 ± 0,01 a 0,97 ± 0,01 sem diferenças nas densidades de 18, 27, 36, 45 e 54 fêmeas/hospedeiro. Esse parasitóide deve ser criado na densidade de 45 fêmeas por pupa de B. mori.

Palavras-chave: hospedeiro alternativo, controle biológico, criação massal, taxas de parasitismo, parasitóides.

INTRODUCTION

The family Eulophidae comprises 297 genera and 4.472 species worldwide. They areendorectoparasitoids; idiobionts or koinobionts; solitary or gregarious; primary or secondary parasitoids; specialists or generalists (Noyes 2003, Pereira et al. 2008b). Many eulophid species are studied and used with success in biological control programs (Gauthier et al. 2000, Pereira et al. 2008a).

Palmistichus elaeisis elvare and LaSalle (Hymenoptera: Eulophidae) is a gregarious endoparasitoid mainly of Lepidoptera pupae. This species was recorded in Brazil in Eupseudosoma involuta (Sepp) (Lepidoptera: Noctuidae) and Euselasia eucerus Hewitson (Lepidoptera: Riodinidae) (Delvare and LaSalle 1993), Sabulodes sp. (Lepidoptera: Geometridae) (Bittencourt and Berti Filho 1999) and Thyrinteina arnobia (Stoll) and Thyrinteina leucoceraea Rindge (Lepidoptera: Geometridae) in eucalyptus plants in the Minas Gerais State, Brazil (Pereira et al. 2008b), being one important natural enemy due to their attack rate (Zanuncio et al. 2009).

The mass rearing represents an important stage of control programs (Parra et al. 2002, Pastori et al. 2008, Pereira et al. 2009), and the nutritional quality, size, age, mechanical resistance and capacity of immunological response of parasitoids should be considered to select alternative hosts (Godfray 1994). P. elaeisis showed a good reproductive performance (adequate parasitism, emergence, progeny per pupa, and size of the body, besides longevity of males and females and sex ratio) when reared on pupae of the alternative host Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae). In addition, the low cost to rear this alternative host indicates that it could be easily used to mass rear the parasitoid P. elaeisis for biological control programs (Zanuncio et al. 2008).

The density of parasitoids per host affects the parasitoid offspring (Thomazini and Berti Filho 2000, Matos Neto et al. 2004), the sex ratio (Choi et al. 2001), the parasitism capacity (Sampaio et al. 2001), the duration of the life cycle, the size of the body, and the longevity of the imagines (Silva-Torres and Matthews 2003). To minimize the cost and labor and to maximize the production of parasitoids in mass rearing programs, it is, therefore, necessary to study the density of the par-asitoids in relation to the host (Sagarra et al. 2000a).

Palmistichus elaeisis are reared on pupae of Diatraea saccharalis (Fabricius) (Lepidoptera: Pyralidae), Anticarsia gemmatalis Hubner, Heliothis virescens (Fa-bricius), Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) and T. arnobia (Bittencourt and Berti Filho 1999, 2004, Pereira et al. 2008b), but the number of females of P. elaeisis per pupae is not known. This is important because P. elaeisis is a gregarious parasitoid, which makes necessary to define the ideal density of its females per pupa of the host to increase the production of descendants with similar quality to native ones.

Bombyx mori L. (Lepidoptera: Bombycidae) has been reared with low cost, and its pupa has high nutritional quality (Greiss et al. 2003, Wang-Dunetal. 2004). For this reason, it can be an adequate host for pupa en-doparasitoids. The objective of this paper was to study the development of P. elaeisis with different numbers of females of this parasitoid per pupae of B. mori.

MATERIALS AND METHODS

The experiment was developed in the Laboratory of Biological Control of the Department of Animal Biology of the "Universidade Federal de Viçosa" (UFV) at Viçosa, Minas Gerais State, Brazil, as:

REARING B. mori

The Sericiculture Laboratory of the Department of Animal Biology (UFV) provided first instar caterpillars of B. mori that were placed in plastic trays (39.3 x 59.5 x 7.0 cm) with Morus alba L leaves, which were changed daily. The pupae obtained of B. mori were transferred to plastic trays (28.3 x 36.0 x 7.0 cm) and placed in an acclimatized chamber at 25 ± 2°C, 70 ± 10% relative humidity (RH) and a photo phase of 12 hours.

REARING THE PARASITOID

Adults of P. elaeisis were kept in glass tubes (14.0 x 2.2 cm) with honey droplets as food. The tubes were closed with a cotton plug. Forty-eight to 72 hours old pupae of B. mori were removed from their cocoons and exposed to the parasitoid females during 24 hours in the acclimatized chamber.

EFFECT OF THE PARASITOID DENSITY ON THE BIOLOGY OF P. elaeisis

Pupae of B. mori (weight 1.06 ± 0.01g) and females of P. elaeisis, both with 72 hours old, at the densities of 1:1, 9:1, 18:1, 27:1, 36:1, 45:1 and 54:1 (parasitoid: host), were reared in an acclimatized chamber at 25 ± 2°C, 70 ± 10% relative humidity (RH) and a photo phase of 12 hours. Each pupa was exposed to the parasitism by females of P. elaeisis into glass tubes (14.0 cm x 2.2 cm) for 24 hours under the conditions user. These females were removed from the tubes at the end of this period.

The parameters evaluated were: the duration of the life cycle (egg-adult), the percentage of parasitism [without the natural mortality of the host (Abbott 1925)], the percentage of emergence of the progeny, the number and size of parasitoids that emerged per pupa, the number of immature that did not complete their development, the sex ratio (which was calculated by the equation SR = number of females/number of males and females). The sex of P. elaeisis was determined by morphologic characteristics in the antenna and the gaster as described by Delvare and LaSalle (1993).

The treatments were represented by the densities of one, nine, 18, 27, 36, 45 and 54 P. elaeisis females per pupa of B. mori in 12 replications in an entirely casualized design. The data of the duration of the life cycle, the number of parasitoids that emerged per pupa and the percentage of dead immature were submitted to a variance analysis. The regression analysis was done with the computer program SigmaPlot 8.0 when the data presented differences at 5% probability. The percentages of parasitism and emergency of P. elaeisis were submitted to the analysis of general linear models (GLM) with binomial distribution (P<0.05) with the computer program R Statistical System (Ihaka and Gentleman 1996). This analysis was carried through with the original data that are not-parametric, but these had been expressed in percentage to facilitate the visualization. The data ofthe sex ratio and those of the size of the body of females and males of P. elaeisis were submitted to a variance analysis and to the test of Scott-Knott with the computer program SAEG 9.0 when they were different at 5% probability.

RESULTS

The density of females of P. elaeisis affected their percentage of parasitism and the number of specimens of this parasitoid that emerged per pupa of B. mori. A total of 72.72% of pupae of this host were parasitized at the density of 1:1, while this number was 100.00% for other densities (P = 0.0312) (Fig. 1). No specimens of P. elaeisis emerged from pupae of B. mori at the densities of 1:1 and 9:1, but those of 45:1 and 54:1 had 100.00% and 54.54% of pupae with parasitoid emergence, respectively (P = 0.0055) (Fig. 1).

The duration of the life cycle (egg-adult) (P = 0.0001; dferror = 30) decreased as the density of P. elaei-sis increased with values from 20 to 28 days (Fig. 2). The density of this parasitoid per pupa of B. mori (F = 4.7025; P = 0.0170; df_error = 31) affected the progeny that was produced. The number of offspring per pupa of B. mori ranged from 49 to 589, but no offspring was produced at the densities 1:1 and 9:1 (Fig. 3). The progeny per female of P. elaeisis per pupa of B. mori was similar, with 18, 27, 36, 45 e 54 females of this parasitoid per pupae of this host (F = 1.2789; P = 0.2674; df_erro = 30) (Fig. 4).

The density of females of P. elaeisis affected the percentage of dead immature of this parasitoid (F = 8.8088; P = 0.0006; df_error = 49) (Fig. 5) with lower numbers (6.83 ± 1.72) at the density of 45:1. The sex ratio of P. elaeisis ranged from 0.93 ± 0.01 to 0.97 ± 0.01, with similar values at all densities (F = 2.12; P = 0.06962) (Table I).

The length of the body of adult P. elaeisis and the width of the head capsule differed among the densities of females of this parasitoid. The length of the body of females and males of P. elaeisis ranged from 1.67 ± 0.04 to 1.89 ± 0.02 mm (F = 3.707; P = 0.00964) and from 1.34 ± 0.01 to 1.54 mm ± 0.03 (F = 5.449; P = 0.00091), respectively (Table I). The width of the head capsule of females and males of P. elaeisis ranged from 0.47 ±0.01 to0.50 ±0.01 mm(F = 3.355; P = 0.01577), and from 0.38 ± 0.01 to 0.44 ± 0.01 mm (F = 4.186; P = 0.00497), with the densities of 18 and 54 females of this parasitoid per pupae of B. mori (Table I).

DISCUSSION

The percentage of parasitism and emergence of P. elaeisis per pupa of B. mori showed that the optimal number of females of this parasitoid per pupae of this host should be 45 for its mass rearing. The progeny of P. elaeisis can be affected by the number of females of P. elaeisis per pupae of B. mori. This indicates that inadequate numbers of females of this parasitoid can reduce the number of eggs laid per host and the amount of toxins injected in the pupa by the female wasps. The toxins are necessary to reduce the immunological response from the pupa, a defense mechanism used by the pupa to encapsulate eggs and/or larvae of the parasitoid (Schmid-Hempel 2005). So, eggs of P. elaeisis may be encapsuled and dead by pupal hemocyts when the female density of this para-sitoid per host is low to suppress the immune response. Nevertheless, high doses of toxins injected by many female P. elaeisis per pupa may kill the host before the complete development of the immature parasitoid occurs (Strand and Pech 1995).

The reproductive parameters of P. elaeisis differed from those of Trichospilus diatraeae Cherian and Mar-gabandhu (Hymenoptera: Eulophidae) and from pupae of D. saccharalis, A. gemmatalis, H. virescens and S. frugiperda exposed to one or several females of this parasitoid. The number of offsprings of T. diatraeae per host almost duplicated, and 100.00% of parasitism was obtained ith several females of this parasitoid per pupa (Paron and Berti Filho 2000). on the other hand, the percentage of parasitism and the emergence of Aphidius colemani Viereck (Hymenoptera: Aphididae) were similar with different densities of Myzus persicae (Sulzer) (Hemiptera: Aphididae). This suggests that M. persicae does not present any nutritional or physiological barriers for the development of A. colemani (Sampaio et al. 2001). B. mori might have an efficient defense mechanism against P. elaeisis because the emergence of this parasitoid was observed only from 18:1 and higher densities of the parasitoid per pupae of this host.

The absence of offsprings of P. elaeisis at the density 1:1 can be due to the encapsulation of its eggs by the immune defense of the pupa of B. mori. This mechanism and the melanization constitute the main defense of insects against strange materials in their bodies (Schmid-Hempel 2005). On the other hand, parasitoids can avoid the encapsulation by injecting particles that are similar to virus, polidnaviroses or poisons into the host to interfere with its immunological recognition (Strand and Pech 1995, Schmidt et al. 2001, Nakamatsu and Tanaka 2003), as well as the depletion of the immune system that has high energy cost, is finite and can be neutralized by toxins from parasitoids (Schmid-Hempel 2005). These hypotheses may explain the high number of P. elaeisis per pupa of B. mori at the in density of 54:1, suggesting that this amount of female parasitoids is sufficient to neutralize the immune response ofthis host. The decrease on parasitoid progeny with the density 54:1 parasitoid:host suggests the occurrence of superparasitism.

The shorter life cycle duration of P. elaeisis in the densities 36:1; 45:1 and 54:1, indicates that the competition for nutrients reduced the development of these immature parasitoids. This agrees with reports for different densities of Melittobia digitata Dahms (Hyme-noptera: Eulophidae) per pupa of Neobellieria bullata Parker (Diptera: Sarcophagidae) (Silva-Torres and Matthews 2003). The duration of the immature stages of P. elaeisis with A. gemmatalis, D. saccharalis, S. frugiperda, T. arnobia and H. virescens was 18.9, 19.5, 19.7, 20.2 and 22.0 days, respectively. These results demonstrate that the host species also affects the development period of this parasitoid (Bittencourt and Berti Filho 2004).

The similar number of progeny per female of P. elaeisis in the densities 18:1, 27:1, 36:1, 45:1 and 54:1, parasitoid:host shows that this natural enemy control the number of eggs per ovipositon and recognizes non parasitized, parasitized or super-parasitized hosts. However, the competition, size and age of the parasitoid, besides the number of eggs encapsulated by the host, can also affect the number of offsprings (Godfray 1994, Sagarra et al. 2000a, b).

The sex ratio of P. elaeisis was similar considering the host T. molitor (Zanuncio et al. 2008) and other eulophid parasitoids such as Melittobia clavicornis Cameron (Gonzáles et al. 2004), Melittobia australica Girault and M. digitata (Silva-Torres and Matthews 2003), suggesting that a high sex ratio is characteristic to Eulophidae.

The smaller size of emerging adult P. elaeisis at the density 54:1 indicates the occurrence of competion for nutrients during the larva stage of this parasitoid. This is important because the size of the body is positively correlated with the longevity, fecundity, reproductive period, emergence of the progeny and sex ratio, which are indicators of quality and efficiency of the parasitoids. Large females and males of Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) lived longer (35.4 ± 10.0; 29.16 ± 6.5 days) than small ones (27.9 ± 9.6; 18.4 ± 5.7 days), respectively, but females of A. kamali to mate with males large rather or small, no preference. However, the fecundity of A. kamali was positively correlated with the size of the females, with values of 37 ± 21 eggs for small females, and 96 ± 43 for large females. The parasitism capacity, daily oviposition rate and the number of offsprings per female of A. kamali showed higher values for large specimens. This suggests the necessity of using larger specimens and to monitor mass rearing facilities in order to maximize the production of parasitoids (Sagarra et al. 2001).

Palmistichus elaeisis parasitized B. mori pupae at the density of 1:1, 9:1, 18:1, 27:1, 36:1, 45:1 and 54:1 (parasitoid: host), but densities below or above 45 para-sitoids per pupa are inadequate for producing lownumber of descendants, besides favoring the auto-immune reply of B. mori pupae. This parasitoid should be reared with the density of 45 females per pupa of B. mori in laboratory and economic studies (Monteiro et al. 2006), and in field (Pratissoli et al. 2005a, b) it must be conducted to be applied in biological control programs.

ACKNOWLEDGMENTS

To Dr. Christer Hansson, Lund University, Sweden and Dr. Marcelo Teixeira Tavares, Universidade Federal do Espírito Santo for the identification of the parasitoid. To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and to Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG).

Manuscript received on March 6, 2009; accepted for publication on July 30, 2009

• ABBOTT WS. 1925. A method of computing the effectiveness of an insecticide. J Econ Entomol 18: 265-267.
• BITTENCOURT MAL AND BERTI FILHO E. 1999. Preferência de Palmistichus elaeisis por pupas de diferentes lepi-dópteros pragas. Scientia Agric 56: 1281-1283.
• BITTENCOURT MAL AND BERTI FILHO E. 2004. Exigências térmicas para o desenvolvimento de Palmistichus elaeisis (Hymenoptera, Eulophidae) em pupas de cinco espécies de lepidópteros. Iheringia Ser Zool 94: 321-323.
• CHOI WI, YOON TJ AND RYOO MI. 2001. Host-size-dependent feeding behaviour and progeny sex ratio of Anisopteroalus calandrae (Hym., Pteromalidae). J Appl Entomol 125: 71-77.
• DELVARE G AND LASALLE J. 1993. A new genus of Tetrastichinae (Hymenoptera: Eulophidae) from the Neotropical region, with the description of a new species parasitic on key pests of oil palm. J Nat Hist 27: 435-444.
• GAUTHIER N, LASALLE J, QUICKE DLJ AND GODFRAY HCJ. 2000. Phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with a reclassification of Eulophinae and the recognition that Elasidae are derived eulophids. Syst Entomol 25: 521-539.
• GODFRAY HCJ. 1994. Parasitoids, behavioral and evolution-aryecology. Princeton: Princeton University Press, 488 p.
• GONZÁLES JM, ABE J AND MATTHEWS RW. 2004. Offspring production and development in the parasitoid wasp Melittobia clavicornis (Cameron) (Hymenoptera: Eulophidae) from Japan. Entomol Science 7: 15-19.
• GREISS H, PETKOV N, BOITCHEV K AND PETKOV Z. 2003. Study on improved technology for silkworm Bobyx ori L. rearing in Egypt. II. Commercial egg production. Bull Jour Agric Science 9: 109-112.
• IHAKA R AND GENTLEMAN R. 1996. R: A language for data analysis and graphics. J Comput Graph Statistics 5: 299-314.
• MATOS NETO FC, CRUZ I, ZANUNCIO JC, SILVA CHO AND PICANÇO MC. 2004. Parasitism by Campoletis flavicincta on Spodoptera frugiperda in corn. Pesq Agropec Bras 39: 1077-1081.
• MONTEIRO LB, SOUZA A AND PASTORI PL. 2006. Comparação econômica entre controle biológico e químico para o manejo de ácaro-vermelho em macieira. Rev Bras Frutic 28: 514-517.
• NAKAMATSU Y AND TANAKA T. 2003. Venom of ectoparasitoid, Euplectrus sp. near plathypenae (Hymenoptera: Eulophidae) regulates the physiological state of Pseudaletia separata (Lepidoptera: Noctuidae) host as a food resource. J Insect Physiol 49: 149-159.
• NOYES J. 2003. Universal Chalcidoidea Database [database on the Internet]. Available from: http:/www.nhm.ac.uk/ researchcuration/projects/chalcids/
• PARON MR AND BERTI FILHO E. 2000. Capacidade reprodutiva de Trichospilus diatraeae (Hymenoptera: Eulophidae) em pupas de diferentes hospedeiros (Lepidoptera). Scientia Agric 57: 355-358.
• PARRA JRP, BOTELHO PSM, CORRÊA-FERREIRA BS AND BENTO JMS. 2002. Controle biológico: Uma visão inter e multidisciplinar, p. 125-137. In: Parra JRP, Botelho PSM, Corrêa-Ferreira BS and Bento JMS (Eds), Controle biológico no Brasil - parasitóides e predadores. Piracicaba: Manole, 609 p.
• PASTORI PL, MONTEIRO LB AND BOTTON M. 2008. Biologia e exigências térmicas de Trichogramma pretiosum Riley (Hymenoptera, Trichogrammatidae) "linhagem bonagota" criado em ovos de Bonagota salubricola (Meyrick) (Lepidoptera, Tortricidae). Rev Bras Entomol 52: 472-476.
• PEREIRA FF, ZANUNCIO JC, TAVARES MT, PASTORI PL, JACQUES GC AND VILELA EF. 2008a. New record of Trichospilus diatraeae as a parasitoid of the eucalypt defoliator Thyrinteina arnobia in Brazil. Phytoparasitica 36: 304-306.
• PEREIRA FF, ZANUNCIO TV, ZANUNCIO JC, PRATISSOLI D AND TAVARES MT. 2008b. Species of Lepidoptera defoliators of eucalypt as new hosts for the polyphagous parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Braz arch biol technol 51: 259-262.
• PEREIRA FF, ZANUNCIO JC, SERRÃO JE, PASTORI PL AND RAMALHO FS. 2009. Reproductive performance of Palmistichus elaeisis (Hymenoptera; Eulophidae) with previously refrigerated pupae of Bombyx mori (Lepidotera; Bombycidae). Braz J Biol 69: 865-869.
• PRATISSOLI D, THULER RT, ANDRADE GS, ZANOTTI LCM AND SILVA AF. 2005a. Estimativa de Trichogramma pretiosum para o controle de Tuta absoluta em tomateiro estaqueado. Pesq Agropec Bras 40: 715-718.
• PRATISSOLI D, VIANA UR, ZAGO HB AND PASTORI PL. 2005b. Capacidade de dispersão de Trichogramma pretiosum em tomate estaqueado. Pesq Agropec Bras 40: 613-616.
• SAGARRA LA, VICENT C AND STEWART RK. 2000a. Mutual interference among female Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) and its impact on fecundity, progeny production and sex ratio. Biocontrol Sci and Tech 10: 239-244.
• SAGARRA LA, PETERKIN DD, VICENT C AND STEWART RK. 2000b. Immune response of the hibiscus mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae), to oviposition of the parasitoid Anagyrus kamali Moursi (Hymenoptera: Encyrtidae). J Insect Physiol 46: 47-653.
• SAGARRA LA, VICENT C AND STEWART RK. 2001. Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bull Entomol Res 91: 363-367.
• SAMPAIO MV, BUENO VHP AND MALUF RP. 2001. Parasitismo de Aphidius colemani Viereck (Hymenoptera: Aphidiidae) em diferentes densidades de Myzus persicae (Sulzer) (Hemiptera: Aphididae). Neotrop Entomol 30: 81-87.
• SCHMID-HEMPEL P. 2005. Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50: 529-551.
• SCHMIDT O, THEOPOLD V AND STRAND MR. 2001. Innate immunity and its evasion and suppression by Hymenoptera endoparasitoid. BioEssays 234: 344-351.
• SILVA-TORRES CSA AND MATTHEWS RW. 2003. Development of Melittobia australica Girault and M. digitata Dahms (Parker) (Hymenoptera: Eulophidae) parasiting Neobellieria bullata (Parker) (Diptera: Sarcophagidae) puparia. Neotrop Entomol 32: 645-651.
• STRAND MR AND PECH LL. 1995. Immunological basis for compatibility in parasitoid-host relationships. Annu Rev Entomol 40: 31-56.
• THOMAZINI MJ AND BERTI FILHO E. 2000. Influência da densidade e idade de pupas de mosca doméstica no parasitismo por Muscidifurax uniraptor (Hymenoptera: Pteromalidae). Rev Agric 75: 339-348.
• WANG-DUN, BAI-YAOYU AND ZHANG-CHUANXI. 2004. A review on the nutritive value of silk worm pupae and its exploitation. Ent Knouw 41: 418-421.
• ZANUNCIO JC, PEREIRA FF, JAQUES GC, TAVARES MT AND SERRÃO JE. 2008. Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), a new alternative host to rear the pupae parasitoid Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae). The Coleopt Bull 62: 64-66.
• ZANUNCIO JC, TORRES JB, SEDIYAMA CAZ, PEREIRA FF, PASTORI PL, WERMELINGER ED AND RAMALHO FS. 2009. Mortality of the defoliator Euselasia eucerus (Lepidoptera: Riodinidae) by biotic factors in an Eucalyptus urophylla plantation in Minas Gerais State, Brazil. An Acad Bras Cienc 81: 61-66.

Publication Dates

• Publication in this collection
  11 June 2010
• Date of issue
  June 2010

History

• Received
  06 Mar 2009
• Accepted
  30 July 2009