Ovary Histology of the Predator Brontocoris tabidus (Hemiptera:Pentatomidae) of Two Ages Fed on Different Diets Author(s) :Walkymário P. Lemos, Virginia V. Zanuncio, Francisco S. Ramalho, José C. Zanuncio, and José E. Serrão Source: Entomological News, 121(3):230-235. 2010. Published By: The American Entomological Society DOI: URL: http://www.bioone.org/doi/full/10.3157/021.121.0303
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OVARY HISTOLOGY OF THE PREDATOR BRONTOCORIS TABIDUS (HEMIPTERA:PENTATOMIDAE) OF TWO AGES FED ON DIFFERENT DIETS1 Walkymário P. Lemos,2 Virginia V. Zanuncio,3 Francisco S. Ramalho,4 José C. Zanuncio,5 and José E. Serrão6 KEY WORDS: Asopinae, Biological control, Histology, Ovary, Zoophytophagy ABSTRACT: The effect of different diets [Tenebrio molitor L. (Coleoptera: Tenebrionidae) pupae without plant; T. molitor pupae and Eucalyptus cloeziana plant; T. molitor pupae and Eucalyptus urophylla plant; T. molitor pupae and guava plant (Psidium guajava)] on the ovary histology of 15 and 21 day old female Brontocoris tabidus (Signoret, 1863) (Hemiptera: Pentatomidae) was analyzed. Females of B. tabidus have ovaries of the meroistic telotrophic type. The vitellarium of this predator presents oocytes with a linear arrangement in different development stages. The follicle cells are cubic with spherical nucleus when the oocytes are placed near the germarium in the initial developmental stage. These cells become flatter and compacted with the development of the oocytes. The ovaries of B. tabidus present similar histological features in all diets and ages. However, females of this predator reared on plants present more oocytes in advanced developmental stages inside the ovarioles than females of same age fed only on prey.
The predator Brontocoris tabidus (Signoret) (Heteroptera: Pentatomidae) is a common and important Asopinae in Brazil (Zanuncio et al., 1994; 1996) because of its high potential for the biological control of Lepidoptera defoliators in forest systems (Jusselino Filho et al., 2001; 2003; Oliveira et al., 2005). The feeding habits on plant and prey by predatory Heteroptera has been studied (Lemos et al., 2001; Zanuncio et al., 2004). The combination of food may supply these predators with essential nutrients lacking in each food resource alone (Eubanks and Denno, 1999) resulting in a positive effect on their biological and reproductive characteristics (Bilde and Toft, 1994; Coll, 1996; 1998; Coll and Izraylevich, 1997; Armer et al., 1998; Eubanks and Denno, 1999; Lemos et al., 2001; Coll and Guershon, 2002; Zanuncio et al., 2004; Fialho et al., 2009). The predator B. tabidus is a zoophytophagous species because it cannot survive for long periods without vegetable material, with both plants and prey in its diet (Zanuncio et al., 2000). This may indicate that the morphology of the repro______________________________ 1
Received on May 20, 2009. Accepted on June 9, 2009.
2
Faculdade de Medicina, Universidade Federal de Juiz de Fora, 36036-330, Juiz de Fora, Minas Gerais, Brazil. E-mail:
[email protected]
3
Laboratório de Entomologia, Embrapa Amazônia Oriental, caixa Postal 048, 66095-100, Belém, Pará, Brazil. E-mail:
[email protected]
4
Unidade de Controle Biológico, EMBRAPA-Algodão, caixa postal 147, 58107-720, Campina Grande, Paraíba, Brazil. E-mail:
[email protected]
5
Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brazil. E-mail:
[email protected]
6
Departamento de Biologia General, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais, Brazil. E-mail:
[email protected] Corresponding author. Mailed on September 28, 2011
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ductive organs of B. tabidus females may be affected by the absence of plants, with a negative impact on its reproduction. The information available, however, is not sufficient to evaluate whether the quality and/or quantity of plant material in the diet affect the histology of the ovary of this predator. This research studied the effects of different diets, of prey only and of prey and two kinds of plants, on the histological features of the ovary of zoophytophage B. tabidus females. METHODS Animals The research was carried out in the field in an area of the Department of Animal Biology and in the laboratories of Biological Control of Insects of the Institute of Applied Biotechnology to the Agriculture (BIOAGRO) and in the laboratories of Molecular and Cell Biology and Reproductive Histology of the Department of General Biology of the Federal University of Viçosa (UFV) in Viçosa, State of Minas Gerais, Brazil, from August 2004 to February 2005. Specimens of B. tabidus were obtained from colonies maintained in the laboratory of Biological Control of Insects of the UFV where this predator is reared in wood-screened cages (30 x 30 x 30 cm) with a glass container with water and Eucalyptus urophylla leaves as vegetable substratum for feeding. The predator which was feeding on Tenebrio molitor L. (Coleoptera: Tenebrionidae) pupae was obtained from the mass rearing facility of the Laboratory of Biological Control of Insects of the UFV. Twenty pairs of B. tabidus were used per treatment with newly emerged adults in the laboratory to obtain the progeny used in the study. Diets Nymphs and adults of B. tabidus were maintained in the field with or without plants in cloth bags (70 cm x 40 cm) (Zanuncio et al., 2004) and fed on T. molitor pupae without plant (T1); T. molitor pupae and Eucalyptus cloeziana plant (T2); T. molitor pupae and Eucalyptus urophylla plant (T3); or T. molitor pupae and guava plant (Psidium guajava) (T4). Five hundred nymphs of B. tabidus were used per diet. These nymphs were obtained from those twenty pairs from the laboratory and they were put in cloth bags to the adult stage. T. molitor pupae were supplied ad libitum and changed with the water twice a week. Nine hundred individuals were used in the T1 due to the high mortality of nymphs of B. tabidus in this treatment, since these nymphs had no access to plants as a food resource. The adults of B. tabidus were sexed on the first day of their emergence based on the external appearance of genitalia, and mated. Thirty-six pairs were formed per treatment. The T1 had 50 pairs due to the high mortality in this treatment. B. tabidus adults received the same prey type and/or plants as the nymphs that they came from. The pairs of this predator were maintained in cloth bags (25 x 15 cm) covering branches of plants with water in a 2.5 ml cylindrical tube (Zanuncio et al., 2004). T. molitor pupae were supplied ad lib. and changed twice
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a week with the water. The cloth bags of the T1 were maintained on the plants but did not cover their branches. Males of the same treatment were substituted for those that died before their respective females. The pair was substituted if the female died before the evaluation date. The number of dead individuals was registered every 48 hours. Histology A total of 10 females 15 and 21 days old of B. tabidus (ages at peak of oviposition) per treatment were obtained from the field and transferred to fixative Zamboni (Stefanini et al., 1967). The ovaries (left and right) of these females were dissected with forceps and maintained in the Zamboni’s fixative solution. The ovaries of B. tabidus were dehydrated in a graded ethanol series and embedded in historesin JB-4®. Sections 5 mm thick were stained with haematoxylin and eosin. RESULTS Brontocoris tabidus has ovaries of the meroistic telotrophic type lined by many layers of a thin epithelium of flat cells and by a muscle layer, the peritoneal sheath (Fig. 1A). The ovariole may be divided in a terminal filament, tropharium (trophic chamber), vitellarium, and pedicel. The germarium area forms the apical part of these ovarioles with cells in differentiation (Fig. 1B). The nurse cells were located in the tropharium with a nutritive cord constituting part of the transport system of nutrients from the nurse cells to the oocytes (Fig. 1C). The remaining parts of the ovariole were formed by the vitellarium where the vitellogenesis and the development of the oocytes take place, which was characterized by oocytes in different developmental stages in a linear arrangement (Fig. 1D). The oocytes were covered by a single layer of follicle cells (Fig. 1D), which was interrupted in the communication point between the nutritive cord and the oocyte. The follicle cells are cubic with a spherical nucleus (Fig. 1E) when the oocytes are located near the germarium. These cells become flatter as the oocytes develop. The follicle cells begin to secrete the eggshell in completely developed oocytes (Fig. 1F). The ovaries have similar histological features in all diets and ages of B. tabidus females. The germarium of B. tabidus females has cells in the process of differentiation, as shown by the cells in metaphase (Fig. 1B). The tropharium also did not present histological differences between the diets consumed by females of B. tabidus. However, oocytes in different developmental stages were found in the vitellarium of females fed without plants (Fig. 1D) with oocytes incompletely developed. However, females reared on plants had a higher quantity of oocytes in advanced stages of development in the ovarioles (Fig. 1F). Females fed on plants (E. cloeziana, E. urophylli, and guava plant) showed follicle cells in differentiation process characterized by the presence of micropylar prolongations in the chorion (Fig. 1F). These structures are visible only in completely developed eggs.
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Fig. 1. Longitudinal section of the ovariole of the predator Brontocoris tabidus (Hemiptera: Pentatomidae) in different stages of development. A, B) germarium region. C) tropharium. D) ovarioles with oocytes in different developmental stages. E, F) details of follicle cells in different stages of development. Arrow, cells in metaphasis; TF, terminal filaments; G, germarium; PS, peritoneal sheath; TR, tropharium; Nc, nutritive cord; Oo, oocyte; NC, nurse cells; FC, follicle cells; n, nucleus; Y, yolk; Vit, vitellarium; Ch, chorion; MP, micropyle prolongations. Scale bars = 20 µm.
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DISCUSSION The meroistic telotrophic ovaries of B. tabidus are the standard type for Hemiptera (Büning, 1994; Simiczyjew et al., 1998; Szklarzewicz, 1998; Adams, 2000 and 2001; Wittmeyer et al., 2001; Lemos et al., 2005). The ovaries of B. tabidus have similar histological characteristics to those of Podisus nigrispinus, a species closely related to this predator (Lemos et al., 2005). The diet consumed affected the development of the ovary and fat body of B. tabidus (Lemos et al., 2009), but not the histological features of the ovaries. Cell differentiation, which shows ovaries were active, characterized the germarium of the ovarioles of B. tabidus females. This differs from that reported for P. nigrispinus females, which showed an advanced degree of cell death when fed an artificial diet (Lemos et al., 2005). Cell death was not observed in any of the tested diets of B. tabidus. Thus plant absence in the diet negatively affects the ovarian development of B. tabidus females resulting in oocyte maturation delay, but it does not cause the death of ovarian cells. We suggest that the presence of plants in the diet is necessary for an adequate ovarian development of B. tabidus, but it does not affect the histological characteristics of the ovaries of this predator. These findings indicate the necessity of additional biochemical studies to evaluate the real effects of the absence of plants in the diet on the reproductive organs and, consequently, on the reproduction of the predator B. tabidus. ACKNOWLEDGMENTS We express thanks to the Brazilian agencies “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).”
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