Oocyte Development in Melanogryllus Desertus (Pallas, 1771) (Orthoptera: Gryllidae): Presence of Balbiani Body*
Total Page：16
File Type：pdf, Size：1020Kb
Turkish Journal of Zoology Turk J Zool (2017) 41: 203-208 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1602-61 Oocyte development in Melanogryllus desertus (Pallas, 1771) (Orthoptera: Gryllidae): presence of Balbiani body* Özlem ÇAKICI** Zoology Section, Department of Biology, Faculty of Science, Ege University, İzmir, Turkey Received: 29.02.2016 Accepted/Published Online: 19.07.2016 Final Version: 04.04.2017 Abstract: Oocyte development in the ovary of the black cricket, Melanogryllus desertus, was investigated. In the panoistic ovary of M. desertus, oocyte developmental stages based on their histological properties were classified as previtellogenic, vitellogenic, and maturation. Oocytes were encircled by follicle cells through the developmental stages. In the previtellogenic stage, a few vacuoles were observed just beneath the oolemma. At the beginning of the vitellogenic stage, subdivided into early-, middle-, and late-vitellogenic stages, yolk granules within the oocyte were initially observed just beneath the oolemma. In addition, small lipid droplets were initially present under the yolk granules. As vitellogenesis proceeded, both yolk granules and lipid droplets gradually increased and moved inside the oocyte. The Balbiani body was detected around the nucleus. In the maturation stage, large yolk granules covering the whole of the oocytes were determined. Some atretic oocytes occurring as a result of resorption of oocytes (oosorption) by hypertrophied follicle cells were also detected. Apoptosis in atretic follicles was observed as well. Key words: Melanogryllus desertus, Gryllidae, Balbiani body, atretic follicle, apoptosis, oosorption 1. Introduction Pentatomidae) (Lemos et al., 2010), Ischnopsyllus spp. Insect ovaries are bilaterally located organs and made (Siphonaptera: Ischnopsyllidae) (Simiczyjew and Margas, up of a number of ovarioles classified as panoistic or 2001), Bactrocera dorsalis (Diptera: Tephritidae) (Chou meroistic (polytrophic and teletrophic). The most et al., 2012), Gryllus yemma (Orthoptera: Gryllidae) primitive ovariole is panoistic type and there are no (Matsuzaki, 1971), and Acheta domesticus (Orthoptera: trophocytes or nurse cells, while the meroistic ovariole Gryllidae) (Dennis and Bradley, 1989). includes both types of cells. Oocytes in panoistic ovariole The Balbiani body is a structure in spherical form are nourished only by the follicular epithelium, while adjacent to the oocyte nucleus in early oogenesis. It nourishment is provided by both follicular cells and disintegrates and disperses within the ooplasm in late trophocytes in the meroistic type (Mazzini, 1987; Singh, oogenesis. This structure has recently been detected in 2007). While panoistic-type ovarioles are present in some insects (Kloc and Etkin, 2005). Among cricket apterygotes, grasshoppers, crickets, termites, dragonflies, species, the Balbiani body has only been determined stoneflies, fleas, and some beetles (Bonhag, 1958; Singh, in the house cricket, Acheta domesticus (Bradley et 2007), meroistic ovarioles are found in flies, moths, and al., 2001). Melanogryllus desertus is a cricket species butterflies (Bradley et al., 2001). commonly called the black cricket. Apart from South There are a number of studies related to the Europe, North Africa, southern parts of Siberia, and ovary morphology in different arthropod species, i.e. Middle Asia, this species is also widely distributed in Amblyomma trieste (Acari: Ixodidae) (de Oliveira et middle and west Anatolia in Turkey (Lodos, 1975). The al., 2006), Rhipicephalus sanguineus (Acari: Ixodidae) present study was designed to determine whether the (de Oliveira et al., 2005), Rhipicephalus microplus Balbiani body is found in the oocytes of M. desertus. To (Acari: Ixodidae) (de Souza, 2013), Elasmucha grisea that end, detailed examinations were conducted using (Heteroptera: Acanthosomatidae) (Ogorzalek and both histochemical and histological methods on oocyte Trochimczuk, 2009), Brontocoris tabidus (Hemiptera: development in M. desertus. * A part of this study was presented at a conference (2nd ICSAE 2015: International Conference on Sustainable Agriculture and En vironment). ** Correspondence: [email protected] 203 ÇAKICI / Turk J Zool 2. Materials and methods with PAS were determined for the first time around the 2.1. Cricket culture periphery of the oocytes in the early vitellogenic stage Black crickets were cultured in laboratory conditions (Figure 2a). As vitellogenesis proceeds, PAS positive (temperature: 26 ± 2 °C; relative humidity: 45 ± 5%; yolk granules cover more and more the oocyte. In the photoperiod: natural). They were maintained in glass meantime, PAS negative lipid droplets were observed in jars by feeding twice a week on lettuce and chicken grain. the ooplasm of these oocytes (Figure 2b). Similarly, yolk Cotton-plugged glass tubes filled with water were put granules reacted with BpB were firstly detected around into these jars to supply the water needs of the crickets. the periphery of the oocytes in the early vitellogenic stage In addition, small petri dishes with their surfaces covered (Figure 3a). In addition, lipid droplets that do not react with moist cotton were placed in the jars for mating with BpB were clearly seen (Figure 3b). On the other hand, females to lay eggs in. The first nymphs emerged within some degenerated oocytes were determined (atresia). In this process, follicle epithelial cells became hypertrophic. 10–12 days. They became adult crickets nine nymphal These cells with many vacuoles resorbed the yolk. This stages later. clearly showed the follicle cells’ phagocytic activity (Figure 2.2. Light microscope analyses 4a). Follicle cells encircled a space formed as a result of Following the dissection of adult females, their ovaries digestion of yolk (oosorption). Moreover, a crescent- were fixed in Bouin’s solution for 24 h. Dehydration was shaped nucleus in the follicle epithelium was determined achieved with graded ethanol (70%, 96%, 100%). Then as an indicator of apoptosis. Some apoptotic bodies around the ovaries were put into xylene to achieve transparency these follicle cells engulfing the oocyte were clearly seen and embedded in paraffin. Thus, fixed tissues were serially (Figure 4b). sectioned at 5-µm thickness using a microtome (Baird & Tatlock). These tissues were stained by Harris Hematoxylin 4. Discussion and Eosin (HE) to reveal general histological organization. Female insects typically produce a large number of eggs to In addition, Periodic Acid Schiff (PAS) and Bromophenol transfer their genes and to that end they invest remarkable Blue (BpB) were used to mark neutral mucosubstances resources (Swevers et al., 2005). In the oogenesis period, (GAGs) and protein in the oocytes, respectively. All proteins, lipids, carbohydrates, and other components are sections were photographed with an Olympus CX 31 regularly deposited in the developing oocyte (Fruttero et photomicroscope. al., 2011). Vitellogenesis is an important process for the maturation of an insect egg. In this period, rapid oocyte 3. Results growth occurs due to yolk deposition (Valle, 1993). Histologic examinations showed that oocytes at different Vitellogenins, which are a group of proteins synthesized stages of oogenesis are found in the ovary of Melanogryllus outside the ovary, are the main component of the yolk and desertus. Oocytes complete their development through stored as vitellin in oocytes (Hagedorn and Kunkel, 1979). three main stages: previtellogenic, vitellogenic, and In the maturation process of oocytes, they become maturation. In the previtellogenic stage, the oocytes are markedly enlarged. Oocytes at different developmental encircled by follicle cells and there are a few vacuoles under stages are present simultaneously in the ovaries of the oolemma (Figure 1a). A large nucleus with prominent Melanogryllus desertus. On the other hand, in the ovaries of nucleolus was determined in these oocytes (Figure 1b). Ambylomma triste, which has panoistic ovaries, there was The vitellogenic stage is subdivided into early-, middle-, no great morphological variation between the oocytes. In and late-vitellogenic stages. In this stage, oocyte volume other words, oocytes develop synchronously (de Oliveira begins to increase. In the early vitellogenic stage, yolk et al., 2006). granules firstly appear just beneath the oolemma. Small Immature oocytes of some invertebrates such as lipid droplets that do not react with H&E were observed chelicerates, myriapods, and insects and of vertebrates such just below the yolk granules (Figure 1c). As vitellogenesis as fish, amphibians, birds, and mammals include a distinct proceeds, both occupy the inside of the oocyte. The Balbiani cytoplasmic organelle called the Balbiani body (Bradley body is a juxtanuclear spherical complex of organelles in et al., 2001; Tworzydlo et al., 2009). Ultrastructurally, developing oocytes of many species (Jaglarz et al., 2003). the Balbiani body is a structure that contains a dense In the middle vitellogenic stage, the Balbiani body was cloud of tubular mitochondria, rough ER, Golgi-like determined around the germinal vesicle (nucleus) (Figure membrane aggregates, and microtubules. Well-developed 1d). In the late vitellogenic stage, many yolk granules Balbiani bodies form adjacent to and on opposite sides of and lipid droplets larger than the previous stage were the germinal vesicle in the oocytes of the house cricket, observed within the oocyte (Figure 1e).