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Notes on the morphology and histology of the ovarioles of Gerris lacustris (L.) (water strider) (Insecta: Hemiptera: Heteroptera: Gerridae)
Zoologischer Anzeiger 278 (2019) 84e89
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Research paper
Notes on the morphology and histology of the ovarioles of Gerris lacustris (L.) (water strider) (Insecta: Hemiptera: Heteroptera: Gerridae) € lu, Selami Candan*, Zekiye Suludere Nurcan Ozyurt Koçakog Biology Department, Faculty of Science, Gazi University, 06500, Ankara, Turkey
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 January 2018 Received in revised form 3 December 2018 Accepted 3 December 2018 Available online 13 December 2018
The morphology and histology of the female reproductive system of Gerris lacustris water strider (Linnaeus 1758) (Heteroptera: Gerridae) are described using both light and scanning electron microscopy (SEM). Based on histomorphology, the adult female reproductive system of G. lacustris consists of a pair of ovaries, a pair of lateral oviducts, a common oviduct. The ovaries are connected to a genital aperture by oviducts. Each adult ovary is composed of four telotrophic meroistic type ovarioles. A peritoneal sheath is a thin membranous layer surrounding the entire ovariole. The ovarioles are attached to the dorsal wall of the anterior prothorax by terminal filaments. Each ovariole is divisible into four different regions: the thread like terminal filament followed by the germarium containing nurse cells (trophocytes) and the primordial oocytes, vitellarium containing oocytes at different developmental stages and pedicel (ovariolar stalk, calyx). A long vitellarium is developed composed of a series of oocytes in their folicular sheath. The vitellarium becomes progressively large towards the distal end and the pedicel, in which the mature eggs are lodged before passing into the short lateral oviduct. It opens to the common oviduct. © 2018 Elsevier GmbH. All rights reserved.
Keywords: Gerridae Ovary Ovariole Histomorphology Light microscope SEM
1. Introduction The Heteroptera are a globally distributed suborder of Hemiptera with very diversified and significant ecological roles (Naranjo et al. 2010). It contains terrestrial, aquatic and semiaquatic species (Novais et al. 2017). According to Polhemus & Polhemus (2008), the aquatic and semi-aquatic Heteroptera, including the infraorders Leptopodomorpha, Gerromorpha, and Nepomorpha, (the last two encompassing approximately 92% of the aquatic bug diversity), comprise an important component of the world's aquatic insect biota. The Gerromorpha (water striders) generally live on the water surface, but rarely under its surface (Polhemus & Polhemus 2008). The group includes water treaders (Mesoveliidae), marsh traders (Hydrometridae), riffle bugs (Veliidae), and water striders (Gerridae) (Zinovjeva 2013). Species in the Gerridae have a worldwide distribution, occurring in all non-polar biogeographic regions (Polhemus & Polhemus 2008).
While there are many publications concerning the female reproductive system in Heteroptera (Ma & Ramaswamy 1987; ski et al. 1990; Jawale & Ranade 1990; Lalitha et al. 1997; Stys Bilin et al. 1998; Szklarzewicz 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel et al. 2006; Uceli et al. € 2011; Ozyurt et al. 2013; Kot et al. 2016; Mattison et al. 2017), none of these have dealt with gerromorphan taxa, a phylogenetically important group. To further understand the evolution and modifications of the female reproductive tract, an examination of gerromorphans was deemed necessary. Morphological and histological characteristics of the female reproductive apparatus and especially the ovariole, have been used to differentiate between families of Heteroptera. On this basis, it was decided to investigate the morphology and histology of the female reproductive system in Gerris lacustris (L.).
2. Material and methods 2.1. Insects
* Corresponding author. € lu), scandan@ E-mail addresses: [email protected] (N. Ozyurt Koçakog gazi.edu.tr (S. Candan), [email protected] (Z. Suludere). https://doi.org/10.1016/j.jcz.2018.12.001 0044-5231/© 2018 Elsevier GmbH. All rights reserved.
Ten adult female specimens of G. lacustris were collected in water-filled containers from lakes in the Kazan district of Ankara
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Province in Turkey between JuneeAugust 2017 and transported to the laboratory of the Department of Biology, University of Gazi, Ankara, Turkey.
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with JEOL JSM 6060 LV scanning electron microscope (JEOL Technics, Ltd, Tokyo, Japan) at accelerating voltages of 5e10 kV. 3. Results
2.2. Light microscopy (LM) The females were dissected in 70% ethyl alcohol for morphological observation and some of the dissected samples were subsequently photographed using a Leica EZ4D stereomicroscope (Germany). For histology, the tissues were fixed in Formaldehyde for 24 h and then washed with tap water. Afterwards the samples were dehydrated in a graded series of ethanol. Following this, they were embedded in paraffin and sectioned at 6e7 mm on a microtome. Sections then were stained with Mallory's Triple. The sections were examined using an Olympus BX51 microscope (Olympus Optical Co. Ltd., Hatagaya, Shibuya-ku, Tokyo, Japan). 2.3. Scanning electron microscopy (SEM) For SEM, other samples were dried in a Critical Point Dryer (Polaron, CPD 7501 England). The dried specimens were mounted with double sided tape on SEM stubs and coated with gold in a Polaron SC 502 sputter coater, and were subsequently examined
The ovaries are located ventro-laterally on each side of the abdomen. Each ovary consisted of four telotrophic ovarioles, with a lateral oviduct emptying into a common oviduct (Fig. 1A and B). Within an ovariole, the terminal filament, germarium (tropharium, trophic chamber), vitellarium, pedicel have been observed (Fig. 1B and D). The present histological study reveals that the oocyte development in the ovarioles of G. lacustris is synchronized (Fig. 1C and D). The ovarioles are attached to the dorsal wall of the anterior prothorax by apical filaments (Fig. 1D). Each ovariole is surrounded by a peritoneal sheath (Figs. 1F and 2B). The germarium (tropharium) area forms the apical part of these ovarioles with cells in differentiation. It contains trophocytes (nurse cells) in its anterior section; primordial oocytes and prefollicular tissue in its posterior (Fig. 1E and F). A large portion of the anterior section of the germarium is occupied by trophocytes. The median region of the germarium contains a trophic core. This region is characterized by the presence of branching strands of cytoplasmic material (trophic core). The nutritive cords in the posterior region of the trophic core,
Fig. 1. A- The appearance of ovary extending from both sides of the digestive canal (SM). B- General view of female internal reproductive system of G. lacustris. Trachea (tr), pedicel (pd), lateral oviduct (lo), common oviduct (co) (SM). C- The longitudinal section of the simultaneously developing oocytes in ovarioles (LM) (X40). D- The germarium (gr), vitellarium (vt) and apical filament (tf) which is connected to the ovaries attached to the body wall (SM). E- The longitudinal section of a germarium. Trophocytes (nurse cells), trophic core (tc), primordial oocytes (po) and prefollicular tissue (pf) (LM) (X100). F- The anterior region of the germarium, trophocytes (tp), peritoneal sheath (ps) (LM) (X400).
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Fig. 2. A-The nutritive cords (nc) joined with the primordial oocytes (po), nucleus (n) (LM) (X400). B, C- In early vitellogenic oocytes, cylindirical folicular epithelial cells (ep) and peritoneal sheath (ps) surrounding the oocytes (LM). D- The trachea (tr) surrounding vitellogenic oocytes in the vitellarium (SEM). E- Light migrograph of the vitellogenic oocyte, epithelium (ep), nucleus (n) (LM) (X400). F- The cubic epithelium (ep) surrounding the late vitellogenic oocyte (SEM).
join with the primordial oocytes (Figs. 1E and 2A). In the most posterior region of the germarium, the primordial oocytes are small and spherical with a single nucleus (Fig. 2A). The remaining parts of the ovariole are formed by the vitellarium where the vitellogenesis and the development of the oocytes take place, characterized by the presence of oocytes in different developmental stages in a linear arrangement (Fig. 2B and C). The oocytes are linked to the tropharium by nutritive cords, which transport nutrients from the anterior nurse cells to each developing oocyte (Figs. 1E and 2A). In the illustration of the young oocytes, the nucleus is spherical and stained strongly with Mallory I (Fig. 2B and E). In G. lacustris, the various developmental stages of oocytes in the vitellarium are previtellogenic, vitellogenic and mature (choreogenic). The oocytes of previtellogenic stage are found in the anterior region of the vitellarium. In previtellogenic oocytes, the follicular epithelium is multilayered (Fig. 2A). In early vitellogenic oocytes, folicular cells surrounding the oocytes are columnar becoming cubic in late vitellogenic stages (Fig. 2B, C, E, 3A) The trachea can be seen on the oocyte surface (Fig. 2D). No morphological differentiation was observed on the vitellogenic oocyte surface (Fig. 2F). In the choreogenic stage, the formation of the chorion layer is completed and the follicular epithelium begins to break down. The oocyte is packed with large yolk spheres. The choriogenic stage is the last stage of the development. The oocyte attains its final size and is surrounded by three layers, which are the vitelline, the chorion and
the squamous follicular epithelium (Fig. 3BeD). In the choreogenic stage, the oocyte has a smooth surface (Fig. 3C). and the pedicel (ovariolar stalk) develops in which the mature eggs are located before passing into the short lateral oviduct, which opens into a short common oviduct (Fig. 3F). The walls of pedicel and those of the lateral oviduct consist of a layer of epithelium cells which are columnar and have a central ovoid nuclei are central in position and ovoid. Externally in the walls, there is a layer of longitudinal muscles (Fig. 3E). The wall of the common oviduct in G. lacustris is surrounded by a single layer of epithelial cells and by muscle bundles (Fig. 4A). The mature oocyte is released from the genital chamber (Fig. 4B). The newly laid eggs are white (Fig. 4C) but subsequently changes colouration as pigmentation starts to occur beneath the chorion (Fig. 4D). The anterior section of an egg contains only one micropyle. In SEM examinations, a slightly collapsed micropylar opening was observed (Fig. 4E). The transverse section of the egg of chorion G. lacustris is composed of exochorion and endochorion (Fig. 4F). The first external evidence of the embryonic development in eggs is the appearance of paired red eye spots next to the micropylar region (Fig. 4D). 4. Discussion Generally, the female reproductive system in Heteroptera consists of paired ovaries, lateral oviducts, a common oviduct and a
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Fig. 3. A- The cubic epithelium (ep) surrounding the late vitellogenic oocyte (SEM). B- The vitelline (vt), the chorion (ch) and the squamous follicular epithelium (ep) in the choriogenic oocyte (LM) (X400). C, D-The choriogenic oocyte surrounding the squamous epithelial layer (ep), the inner surface of epithelial layer in oocyte (SEM). E- The connection of pedicel (pd) with the lateral oviducts (lo), muscle structure (ms) (LM) (X200). F- The connection of pedicel (pd) with the lateral oviducts (lo), common oviduct (co) (SEM).
spermatheca. In each ovariole, there is a terminal filament preceding a germarium, which is connected to a vitellarium and a pedicel (ovariolar stalk, calyx). The germarium contains trophocytes (nurse cells), primordial oocytes and prefollicular cells. The oocytes in the vitellarium are connected to trophocytes by nutritive cords and by cytoplasmic projections. The ovarioles are linked to the lateral oviduct by the pedicel. Both lateral oviducts converge and form a median common oviduct which is continuous posteriorly with the vagina and opens into the genital chamber (Pendergrast 1957; Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo € Lemos et al. 2005; Hummel et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). When a spermatheca, is present it arises from the dorsal wall of this duct (Pendergrast 1957). According to Pendergrast (1957). Gerridae have a spermatheca of a type not found elsewhere in the suborder. The organ consists of a basal spermathecal bulb, which is in direct communication with the vagina, and an extremely long narrow apical tube much folded and imbedded in a mass of glandular cells and fat body. In the Gerridae the arrangement of the spermatheca and fecundation canal is more complex than in the other families, although the same elements are present. A large portion of the anterior section of the germarium is occupied by trophocytes, the apical position of the trophocytes is typical of the Hemiptera-Heteroptera and for this reason the ovarioles of these insects are termed telotrophic ovarioles (Ma &
Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Szklarzewicz 1998; de Paulo Lemos et al. 2005; Hummel et al. € ^ nsoli 2014; Kot et al. 2016; 2006; Ozyurt et al. 2013; Dossi & Co Mattison et al. 2017). The female reproductive organs of most Heteroptera are, except for details of the spermatheca, of somewhat uniform character. There are two laterally-placed ovaries of the acrotrophic type, each consisting of a number of ovarioles. The general organization of the female reproductive system in G. lacustris is similar with other studied Heteroptera (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo € Lemos et al. 2005; Hummel et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). Each ovary in Heteroptera consists usually of 3e7 telotrophic ovarioles, but sometimes the number of ovarioles in each ovary may reach 17 (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel et al. 2006; Uceli € et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017) as shown in Table 1. In G. lacustris, there are four telotrophic ovarioles per ovary. Athough families may be characterised by the prevailing ovariole numbers, there are exceptions (Woodward 1950). For example, in the Pentatomidae seven ovarioles are common, but six and four have also been reported. Even within a single genus differences have been observed (Pendergrast 1957).
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Fig. 4. A- The muscle structure (ms) and epithelium(ep) surrounding the common oviduct (LM) (X400). B- The fertilized egg in vagina (SEM). C- The fertilized egg left out of the genital chamber (LM). D- Red eye (re) spots in the embryonic development in eggs (LM). E- The micropyle (m) region in the egg surface (SEM). F- The endochorion layer (en) and the exochorion layer (ex) in the cross section of the egg (SEM). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)
Table 1 The ovariole numbers for Heteroptera-Hemiptera species as reported in the literature. Species-Family
The ovarioles number each ovary
Citation
Gerris lacustris (Linnaeus 1758) (Heteroptera: Gerridae) Lygus lineoralis (Palisot de Beauvois) (Heteroptera: Miridae) Sphaerodema (Diplonychus) rusticum (Fabricius) (Heteroptera: Belostomatidae) Abedus ovatus Stål 1862 (Heteroptera: Belostomatidae) Cryptostemma alienum Herrich-Schaeffer, 1835 (Heteroptera: Dipsocoridae) Cryptostemma carpaticum Josifov, 1967 (Heteroptera: Dipsocoridae) Dysmicoccus newsteadi Lagowska and Koteja, 1996 (Hemiptera: Pseudococcidae) Kermes quercus (Linnaeus, 1758) (Hemiptera: Kermesidae) Eriococcus buxi (Boyer de Fonscolombe, 1834) (Hemiptera: Eriococcidae) Gossyparia spuria Modeer 1778 (Hemiptera: Eriococcidae) Cryptococcus fagisuga Lindinger 1936 (Hemiptera: Cryptococcidae) Pseudochermes fraxini (Kaltenbach, 1860) (Hemiptera: Cryptococcidae) Orthezia urticae (Linnaeus, 1758) (Hemiptera: Coccinea) Macroscytus vietnamicus Fieber, 1860 (Heteroptera: Cydnidae) th, 1881) (Heteroptera: Cydnidae) Canthophorus impressus (Horva Tritomegas bicolor (Linnaeus, 1758) (Heteroptera: Cydnidae) Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) Homalodisca coagulata (Say) (Hemiptera: Cicadellidae) Adparaproba gabrieli (Linnaeus, 1758) (Heteroptera: Miridae) Graphosoma lineatum (Linnaeus 1758) (Heteroptera: Pentatomidae) Diaphorina citri Kuwayama (Hemiptera: Psyllidae) Megamelus scutellaris Berg (Hemiptera: Delphacidae)
4 7 5 5 5 5 50e100 50e100 50e100 50e100 50e100 50e100 15 7 7 7 7 10 3 7 nearly 25 11e13
Ma and Ramaswamy (1987) Jawale and Ranade (1990) Lalitha et al. (1997) Stys et al. (1998) Stys et al. (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Vogelsang and Szklarzewicz (2001) Lis (2003) Lis (2003) Lis (2003) de Paulo Lemos et al. (2005) Hummel et al. (2006) Uceli et al. (2011) € Ozyurt et al. (2013) ^nsoli (2014) Dossi and Co Mattison et al. (2017)
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The ovaries of G. lacustris, as in other Heteroptera, are meroistic telotrophic, that is, follicular cells, as well as nurse cells, and oocytes are located in the germarium (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Caperucci & Camargo-Mathias 2006; Hummel et al. 2006; Uceli et al. 2011; Mattison et al. 2017). The functions of the germarium of telotrophic ovarioles are detailed by Jawale & Ranade (1990) for Sphaerodema (Diplonychus) rusticum, by Lalitha et al. (1997) for Abedus ovatus and by Hummel et al. (2006) for Homalodisca coagulata. The primordial oocytes of G. lacustris form attachments to the nutritive cords as they exit the germarium region, as similarly described for Lygus lineolaris (Ma & Ramaswamy 1987), H. coagulata ^nsoli 2014). The (Hummel et al. 2006) and Diaphorina citri (Dossi & Co arrangement of the nuclei around the central trophic core of G. lacustris is similar to that seen in H. coagulata (Hummel et al. 2006). Nijhout (1994) suggested that the process of the development of eggs in the ovariole can be divided into three stages: first, the oocyte undergoes a period of previtellogenic growth with accumulation of proteins, carbohydrates and other nutrients. Then, it is followed by a period of vitellogenesis, during which the oocytes specifically accumulate vitellogenine from the haemolymph. The final stage is choriogenesis, in which the proteinaceous eggshell (chorion) is secreted around the oocyte. Follicular cells are responsible for controlling the access of proteins and nutrients to the oocytes for secretion of the chorion. The histology of the development of the ovaries of G. lacustris is synchronised, as similarly described in H. coagulata (Hummel et al. € 2006) and Graphosoma lineatum (Ozyurt et al. 2013). Our observation is that each ovary contains 4 ovarioles. The pedicel of the ovarioles in G. lacustris, opens into the apical bulb of their respective lateral oviducts. The walls of the pedicel and lateral oviduct in G. lacustris is surrounded by a single layer epithelium of cylindirical cells whereas in S. rusticum the pedicel is composed of simple cuboidal cells (Jawale & Ranade 1990), and in A. ovatus. the epithelial cell is squamous (Lalitha et al. 1997). The epithelial nuclei are ovoid in these species (Jawale & Ranade 1990; Lalitha et al. 1997). In G. lacustris as in S. rusticum, epithelial cells are enveloped by a layer of muscle (Jawale & Ranade 1990). In G. lacustris, as other Heteroptera, the common oviduct, also known as the median oviduct, is formed by the merging of the paired lateral oviducts. The common oviduct opens posteriorly into a genital chamber or vagina (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel € et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). This study provides information on the female reproductive system histomorphology of G. lacustris. These findings will contribute to future studies on the diversity of the reproductive histomorphology in female Heteroptera. Acknowledgments We also thank Dr. Robert Lavigne (Professor Emeritus, University of Wyoming, Laramie, Wyoming, U.S.A.), who revised the grammar of this article.
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References ski, S.M., Ksiazkiewicz-Kapralska, _ Bilin M., Stys, P., 1990. Unusual organization of the tropharium in the telotrophic ovarioles of an insect, Saldula saltatoria. Tissue Cell 22 (2), 213e219. Caperucci, D., Camargo-Mathias, M.I., 2006. Ultrastructural study of the ovary of the sugarcane spittlebug Mahanarva fimbriolata (Hemiptera). Micron 37 (7), 633e639. ~o, J.E., Zanuncio, J.C., 2005. Morphology of De Paulo Lemos, W., Ramalho, F.D.S., Serra female reproductive tract of the predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) fed on different diets. Braz. Arch. Biol. Technol. 48 (1), 129e138. ^ nsoli, F.L., 2014. Gross morphology and ultrastructure of the female Dossi, F.C.A., Co reproductive system of Diaphorina citri (Hemiptera: Liviidae). Zoologia (Curitiba) 31 (2), 162e169. Hummel, N.A., Zalom, F.G., Peng, C.Y., 2006. Anatomy and histology of reproductive organs of female Homalodisca coagulata (Hemiptera: Cicadellidae: Proconiini), with special emphasis on categorization of vitellogenic oocytes. Ann. Entomol. Soc. Am. 99 (5), 920e932. Jawale, S.M., Ranade, D.R., 1990. Morphology of the ovaries of Sphaerodema (Diplonychus) rusticum (Heteroptera, Belostomatidae). J. Morphol. 205 (2), 183e192. Kot, M., Büning, J., Jankowska, W., Drohojowska, J., Szklarzewicz, T., 2016. Development of ovary structures in the last larval and adult stages of psyllids (Insecta, Hemiptera, Sternorrhyncha: Psylloidea). Arthropod Struct. Dev. 45 (4), 389e398. Lalitha, T.G., Shyamasundari, K., Rao, K.H., 1997. Morphology and histology of the female reproductive system of Abedus ovatus STAL (Belostomatidae: Hemiptera: Insecta). Mem. Inst. Oswaldo Cruz 92, 129e135. Lis, J.A., 2003. Ovaries and lateral oviducts of the female internal reproductive system in five species of burrower bugs (Hemiptera: Heteroptera: Cydnidae). Pol. Pismo Entomol. 72 (4), 305e312. Ma, W.K., Ramaswamy, S.B., 1987. Histological changes during ovarian maturation in the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois)(Hemiptera: Miridae). Int. J. Insect Morphol. Embryol. 16 (5e6), 309e322. Mattison, E., Center, T.D., Grodowitz, M.J., Tipping, P.W., 2017. Morphology of the female reproductive system and physiological age-grading of Megamelus scutellaris (Hemiptera: Delphacidae), a biological control agent of water hyacinth. Fla. Entomol. 100 (2), 303e309. ~ oz Riviaux, S., Moreira, F.F.F., Correa Court, R., 2010. Taxonomy and Naranjo, C., Mun distribution of aquatic and semiaquatic Heteroptera (Insecta) from Cuba. Rev. Biol. Trop. (International Journal of Tropical Biology) 58 (3), 897e907. Nijhout, H.F., 1994. Insect Hormone. University Press, Princeton, New Jersey. Novais, A.M., Dias, G., Lino-Neto, J., 2017. Testicular, spermatogenesis and sperm morphology in Martarega bentoi (Heteroptera: Notonectidae). Arthropod Struct. Dev. 46, 635e643. € Ozyurt, N., Candan, S., Suludere, Z., 2013. The morphology and histology of the female reproductive system of Graphosoma lineatum (Heteroptera: Pentatomidae) based on light and scanning electron microscope studies. Int. J. Sci. Res. 12 (2), 42e46. Pendergrast, J.G., 1957. Studies on the reproductive organs of the Heteroptera with a consideration of their bearing on classification. Ecol. Entomol. 109 (1), 1e63. Polhemus, J.T., Polhemus, Dan A., 2008. Global diversity of true bugs (Heteroptera; Insecta) in freshwater. Hydrobiologia 595 (1), 379e391. ski, S.M., 1998. Organization of the tropharia in the teloStys, P., Büning, J., Bilin trophic ovaries of the dipsocoromorphan bugs Cryptostemma alienum HerrichSchaeffer and C. carpaticum Josifov (Heteroptera: Dipsocoridae). Int. J. Insect Morphol. Embryol. 27 (2), 129e133. Szklarzewicz, T., 1998. Structure of ovaries in scale insects. i. pseudococcidae, kermesidae, eriococcidae, and cryptococcidae (Insecta, Hemiptera, Coccinea). Int. J. Insect Morphol. Embryol. 27 (3), 167e172. Uceli, L.F., Pirovani, V.D., de Freitas Vicente, N.M., Pikart, T.G., Ferreira, P.S.F., ~o, J.E., 2011. Morphology of the reproductive and digestive tracts of Serra Adparaproba gabrieli (Heteroptera: Miridae). Int. J. Trop. Insect Sci. 31 (4), 219e224. Vogelgesang, M., Szklarzewicz, T., 2001. Formation and structure of egg capsules in scale insects (Hemiptera, Coccinea): I. Ortheziidae. Arthropod Struct. Dev. 30 (1), 63e68. Woodward, T.E., 1950. Ovariole and testis follicle numbers in the Heteroptera. Ent. mon. mag. 86, 82e84. Zinovjeva, A.N., 2013. Distribution of water bugs (Heteroptera: Nepomorpha, Gerromorpha) over latitudinal zones in the northeast of European Russia. Inland Water Biol 6 (3), 220e227.
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Zoologischer Anzeiger journal homepage: www.elsevier.com/locate/jcz
Research paper
Notes on the morphology and histology of the ovarioles of Gerris lacustris (L.) (water strider) (Insecta: Hemiptera: Heteroptera: Gerridae) € lu, Selami Candan*, Zekiye Suludere Nurcan Ozyurt Koçakog Biology Department, Faculty of Science, Gazi University, 06500, Ankara, Turkey
a r t i c l e i n f o
a b s t r a c t
Article history: Received 19 January 2018 Received in revised form 3 December 2018 Accepted 3 December 2018 Available online 13 December 2018
The morphology and histology of the female reproductive system of Gerris lacustris water strider (Linnaeus 1758) (Heteroptera: Gerridae) are described using both light and scanning electron microscopy (SEM). Based on histomorphology, the adult female reproductive system of G. lacustris consists of a pair of ovaries, a pair of lateral oviducts, a common oviduct. The ovaries are connected to a genital aperture by oviducts. Each adult ovary is composed of four telotrophic meroistic type ovarioles. A peritoneal sheath is a thin membranous layer surrounding the entire ovariole. The ovarioles are attached to the dorsal wall of the anterior prothorax by terminal filaments. Each ovariole is divisible into four different regions: the thread like terminal filament followed by the germarium containing nurse cells (trophocytes) and the primordial oocytes, vitellarium containing oocytes at different developmental stages and pedicel (ovariolar stalk, calyx). A long vitellarium is developed composed of a series of oocytes in their folicular sheath. The vitellarium becomes progressively large towards the distal end and the pedicel, in which the mature eggs are lodged before passing into the short lateral oviduct. It opens to the common oviduct. © 2018 Elsevier GmbH. All rights reserved.
Keywords: Gerridae Ovary Ovariole Histomorphology Light microscope SEM
1. Introduction The Heteroptera are a globally distributed suborder of Hemiptera with very diversified and significant ecological roles (Naranjo et al. 2010). It contains terrestrial, aquatic and semiaquatic species (Novais et al. 2017). According to Polhemus & Polhemus (2008), the aquatic and semi-aquatic Heteroptera, including the infraorders Leptopodomorpha, Gerromorpha, and Nepomorpha, (the last two encompassing approximately 92% of the aquatic bug diversity), comprise an important component of the world's aquatic insect biota. The Gerromorpha (water striders) generally live on the water surface, but rarely under its surface (Polhemus & Polhemus 2008). The group includes water treaders (Mesoveliidae), marsh traders (Hydrometridae), riffle bugs (Veliidae), and water striders (Gerridae) (Zinovjeva 2013). Species in the Gerridae have a worldwide distribution, occurring in all non-polar biogeographic regions (Polhemus & Polhemus 2008).
While there are many publications concerning the female reproductive system in Heteroptera (Ma & Ramaswamy 1987; ski et al. 1990; Jawale & Ranade 1990; Lalitha et al. 1997; Stys Bilin et al. 1998; Szklarzewicz 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel et al. 2006; Uceli et al. € 2011; Ozyurt et al. 2013; Kot et al. 2016; Mattison et al. 2017), none of these have dealt with gerromorphan taxa, a phylogenetically important group. To further understand the evolution and modifications of the female reproductive tract, an examination of gerromorphans was deemed necessary. Morphological and histological characteristics of the female reproductive apparatus and especially the ovariole, have been used to differentiate between families of Heteroptera. On this basis, it was decided to investigate the morphology and histology of the female reproductive system in Gerris lacustris (L.).
2. Material and methods 2.1. Insects
* Corresponding author. € lu), scandan@ E-mail addresses: [email protected] (N. Ozyurt Koçakog gazi.edu.tr (S. Candan), [email protected] (Z. Suludere). https://doi.org/10.1016/j.jcz.2018.12.001 0044-5231/© 2018 Elsevier GmbH. All rights reserved.
Ten adult female specimens of G. lacustris were collected in water-filled containers from lakes in the Kazan district of Ankara
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Province in Turkey between JuneeAugust 2017 and transported to the laboratory of the Department of Biology, University of Gazi, Ankara, Turkey.
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with JEOL JSM 6060 LV scanning electron microscope (JEOL Technics, Ltd, Tokyo, Japan) at accelerating voltages of 5e10 kV. 3. Results
2.2. Light microscopy (LM) The females were dissected in 70% ethyl alcohol for morphological observation and some of the dissected samples were subsequently photographed using a Leica EZ4D stereomicroscope (Germany). For histology, the tissues were fixed in Formaldehyde for 24 h and then washed with tap water. Afterwards the samples were dehydrated in a graded series of ethanol. Following this, they were embedded in paraffin and sectioned at 6e7 mm on a microtome. Sections then were stained with Mallory's Triple. The sections were examined using an Olympus BX51 microscope (Olympus Optical Co. Ltd., Hatagaya, Shibuya-ku, Tokyo, Japan). 2.3. Scanning electron microscopy (SEM) For SEM, other samples were dried in a Critical Point Dryer (Polaron, CPD 7501 England). The dried specimens were mounted with double sided tape on SEM stubs and coated with gold in a Polaron SC 502 sputter coater, and were subsequently examined
The ovaries are located ventro-laterally on each side of the abdomen. Each ovary consisted of four telotrophic ovarioles, with a lateral oviduct emptying into a common oviduct (Fig. 1A and B). Within an ovariole, the terminal filament, germarium (tropharium, trophic chamber), vitellarium, pedicel have been observed (Fig. 1B and D). The present histological study reveals that the oocyte development in the ovarioles of G. lacustris is synchronized (Fig. 1C and D). The ovarioles are attached to the dorsal wall of the anterior prothorax by apical filaments (Fig. 1D). Each ovariole is surrounded by a peritoneal sheath (Figs. 1F and 2B). The germarium (tropharium) area forms the apical part of these ovarioles with cells in differentiation. It contains trophocytes (nurse cells) in its anterior section; primordial oocytes and prefollicular tissue in its posterior (Fig. 1E and F). A large portion of the anterior section of the germarium is occupied by trophocytes. The median region of the germarium contains a trophic core. This region is characterized by the presence of branching strands of cytoplasmic material (trophic core). The nutritive cords in the posterior region of the trophic core,
Fig. 1. A- The appearance of ovary extending from both sides of the digestive canal (SM). B- General view of female internal reproductive system of G. lacustris. Trachea (tr), pedicel (pd), lateral oviduct (lo), common oviduct (co) (SM). C- The longitudinal section of the simultaneously developing oocytes in ovarioles (LM) (X40). D- The germarium (gr), vitellarium (vt) and apical filament (tf) which is connected to the ovaries attached to the body wall (SM). E- The longitudinal section of a germarium. Trophocytes (nurse cells), trophic core (tc), primordial oocytes (po) and prefollicular tissue (pf) (LM) (X100). F- The anterior region of the germarium, trophocytes (tp), peritoneal sheath (ps) (LM) (X400).
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Fig. 2. A-The nutritive cords (nc) joined with the primordial oocytes (po), nucleus (n) (LM) (X400). B, C- In early vitellogenic oocytes, cylindirical folicular epithelial cells (ep) and peritoneal sheath (ps) surrounding the oocytes (LM). D- The trachea (tr) surrounding vitellogenic oocytes in the vitellarium (SEM). E- Light migrograph of the vitellogenic oocyte, epithelium (ep), nucleus (n) (LM) (X400). F- The cubic epithelium (ep) surrounding the late vitellogenic oocyte (SEM).
join with the primordial oocytes (Figs. 1E and 2A). In the most posterior region of the germarium, the primordial oocytes are small and spherical with a single nucleus (Fig. 2A). The remaining parts of the ovariole are formed by the vitellarium where the vitellogenesis and the development of the oocytes take place, characterized by the presence of oocytes in different developmental stages in a linear arrangement (Fig. 2B and C). The oocytes are linked to the tropharium by nutritive cords, which transport nutrients from the anterior nurse cells to each developing oocyte (Figs. 1E and 2A). In the illustration of the young oocytes, the nucleus is spherical and stained strongly with Mallory I (Fig. 2B and E). In G. lacustris, the various developmental stages of oocytes in the vitellarium are previtellogenic, vitellogenic and mature (choreogenic). The oocytes of previtellogenic stage are found in the anterior region of the vitellarium. In previtellogenic oocytes, the follicular epithelium is multilayered (Fig. 2A). In early vitellogenic oocytes, folicular cells surrounding the oocytes are columnar becoming cubic in late vitellogenic stages (Fig. 2B, C, E, 3A) The trachea can be seen on the oocyte surface (Fig. 2D). No morphological differentiation was observed on the vitellogenic oocyte surface (Fig. 2F). In the choreogenic stage, the formation of the chorion layer is completed and the follicular epithelium begins to break down. The oocyte is packed with large yolk spheres. The choriogenic stage is the last stage of the development. The oocyte attains its final size and is surrounded by three layers, which are the vitelline, the chorion and
the squamous follicular epithelium (Fig. 3BeD). In the choreogenic stage, the oocyte has a smooth surface (Fig. 3C). and the pedicel (ovariolar stalk) develops in which the mature eggs are located before passing into the short lateral oviduct, which opens into a short common oviduct (Fig. 3F). The walls of pedicel and those of the lateral oviduct consist of a layer of epithelium cells which are columnar and have a central ovoid nuclei are central in position and ovoid. Externally in the walls, there is a layer of longitudinal muscles (Fig. 3E). The wall of the common oviduct in G. lacustris is surrounded by a single layer of epithelial cells and by muscle bundles (Fig. 4A). The mature oocyte is released from the genital chamber (Fig. 4B). The newly laid eggs are white (Fig. 4C) but subsequently changes colouration as pigmentation starts to occur beneath the chorion (Fig. 4D). The anterior section of an egg contains only one micropyle. In SEM examinations, a slightly collapsed micropylar opening was observed (Fig. 4E). The transverse section of the egg of chorion G. lacustris is composed of exochorion and endochorion (Fig. 4F). The first external evidence of the embryonic development in eggs is the appearance of paired red eye spots next to the micropylar region (Fig. 4D). 4. Discussion Generally, the female reproductive system in Heteroptera consists of paired ovaries, lateral oviducts, a common oviduct and a
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Fig. 3. A- The cubic epithelium (ep) surrounding the late vitellogenic oocyte (SEM). B- The vitelline (vt), the chorion (ch) and the squamous follicular epithelium (ep) in the choriogenic oocyte (LM) (X400). C, D-The choriogenic oocyte surrounding the squamous epithelial layer (ep), the inner surface of epithelial layer in oocyte (SEM). E- The connection of pedicel (pd) with the lateral oviducts (lo), muscle structure (ms) (LM) (X200). F- The connection of pedicel (pd) with the lateral oviducts (lo), common oviduct (co) (SEM).
spermatheca. In each ovariole, there is a terminal filament preceding a germarium, which is connected to a vitellarium and a pedicel (ovariolar stalk, calyx). The germarium contains trophocytes (nurse cells), primordial oocytes and prefollicular cells. The oocytes in the vitellarium are connected to trophocytes by nutritive cords and by cytoplasmic projections. The ovarioles are linked to the lateral oviduct by the pedicel. Both lateral oviducts converge and form a median common oviduct which is continuous posteriorly with the vagina and opens into the genital chamber (Pendergrast 1957; Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo € Lemos et al. 2005; Hummel et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). When a spermatheca, is present it arises from the dorsal wall of this duct (Pendergrast 1957). According to Pendergrast (1957). Gerridae have a spermatheca of a type not found elsewhere in the suborder. The organ consists of a basal spermathecal bulb, which is in direct communication with the vagina, and an extremely long narrow apical tube much folded and imbedded in a mass of glandular cells and fat body. In the Gerridae the arrangement of the spermatheca and fecundation canal is more complex than in the other families, although the same elements are present. A large portion of the anterior section of the germarium is occupied by trophocytes, the apical position of the trophocytes is typical of the Hemiptera-Heteroptera and for this reason the ovarioles of these insects are termed telotrophic ovarioles (Ma &
Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Szklarzewicz 1998; de Paulo Lemos et al. 2005; Hummel et al. € ^ nsoli 2014; Kot et al. 2016; 2006; Ozyurt et al. 2013; Dossi & Co Mattison et al. 2017). The female reproductive organs of most Heteroptera are, except for details of the spermatheca, of somewhat uniform character. There are two laterally-placed ovaries of the acrotrophic type, each consisting of a number of ovarioles. The general organization of the female reproductive system in G. lacustris is similar with other studied Heteroptera (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo € Lemos et al. 2005; Hummel et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). Each ovary in Heteroptera consists usually of 3e7 telotrophic ovarioles, but sometimes the number of ovarioles in each ovary may reach 17 (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel et al. 2006; Uceli € et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017) as shown in Table 1. In G. lacustris, there are four telotrophic ovarioles per ovary. Athough families may be characterised by the prevailing ovariole numbers, there are exceptions (Woodward 1950). For example, in the Pentatomidae seven ovarioles are common, but six and four have also been reported. Even within a single genus differences have been observed (Pendergrast 1957).
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Fig. 4. A- The muscle structure (ms) and epithelium(ep) surrounding the common oviduct (LM) (X400). B- The fertilized egg in vagina (SEM). C- The fertilized egg left out of the genital chamber (LM). D- Red eye (re) spots in the embryonic development in eggs (LM). E- The micropyle (m) region in the egg surface (SEM). F- The endochorion layer (en) and the exochorion layer (ex) in the cross section of the egg (SEM). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)
Table 1 The ovariole numbers for Heteroptera-Hemiptera species as reported in the literature. Species-Family
The ovarioles number each ovary
Citation
Gerris lacustris (Linnaeus 1758) (Heteroptera: Gerridae) Lygus lineoralis (Palisot de Beauvois) (Heteroptera: Miridae) Sphaerodema (Diplonychus) rusticum (Fabricius) (Heteroptera: Belostomatidae) Abedus ovatus Stål 1862 (Heteroptera: Belostomatidae) Cryptostemma alienum Herrich-Schaeffer, 1835 (Heteroptera: Dipsocoridae) Cryptostemma carpaticum Josifov, 1967 (Heteroptera: Dipsocoridae) Dysmicoccus newsteadi Lagowska and Koteja, 1996 (Hemiptera: Pseudococcidae) Kermes quercus (Linnaeus, 1758) (Hemiptera: Kermesidae) Eriococcus buxi (Boyer de Fonscolombe, 1834) (Hemiptera: Eriococcidae) Gossyparia spuria Modeer 1778 (Hemiptera: Eriococcidae) Cryptococcus fagisuga Lindinger 1936 (Hemiptera: Cryptococcidae) Pseudochermes fraxini (Kaltenbach, 1860) (Hemiptera: Cryptococcidae) Orthezia urticae (Linnaeus, 1758) (Hemiptera: Coccinea) Macroscytus vietnamicus Fieber, 1860 (Heteroptera: Cydnidae) th, 1881) (Heteroptera: Cydnidae) Canthophorus impressus (Horva Tritomegas bicolor (Linnaeus, 1758) (Heteroptera: Cydnidae) Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) Homalodisca coagulata (Say) (Hemiptera: Cicadellidae) Adparaproba gabrieli (Linnaeus, 1758) (Heteroptera: Miridae) Graphosoma lineatum (Linnaeus 1758) (Heteroptera: Pentatomidae) Diaphorina citri Kuwayama (Hemiptera: Psyllidae) Megamelus scutellaris Berg (Hemiptera: Delphacidae)
4 7 5 5 5 5 50e100 50e100 50e100 50e100 50e100 50e100 15 7 7 7 7 10 3 7 nearly 25 11e13
Ma and Ramaswamy (1987) Jawale and Ranade (1990) Lalitha et al. (1997) Stys et al. (1998) Stys et al. (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Szklarzewicz (1998) Vogelsang and Szklarzewicz (2001) Lis (2003) Lis (2003) Lis (2003) de Paulo Lemos et al. (2005) Hummel et al. (2006) Uceli et al. (2011) € Ozyurt et al. (2013) ^nsoli (2014) Dossi and Co Mattison et al. (2017)
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The ovaries of G. lacustris, as in other Heteroptera, are meroistic telotrophic, that is, follicular cells, as well as nurse cells, and oocytes are located in the germarium (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Caperucci & Camargo-Mathias 2006; Hummel et al. 2006; Uceli et al. 2011; Mattison et al. 2017). The functions of the germarium of telotrophic ovarioles are detailed by Jawale & Ranade (1990) for Sphaerodema (Diplonychus) rusticum, by Lalitha et al. (1997) for Abedus ovatus and by Hummel et al. (2006) for Homalodisca coagulata. The primordial oocytes of G. lacustris form attachments to the nutritive cords as they exit the germarium region, as similarly described for Lygus lineolaris (Ma & Ramaswamy 1987), H. coagulata ^nsoli 2014). The (Hummel et al. 2006) and Diaphorina citri (Dossi & Co arrangement of the nuclei around the central trophic core of G. lacustris is similar to that seen in H. coagulata (Hummel et al. 2006). Nijhout (1994) suggested that the process of the development of eggs in the ovariole can be divided into three stages: first, the oocyte undergoes a period of previtellogenic growth with accumulation of proteins, carbohydrates and other nutrients. Then, it is followed by a period of vitellogenesis, during which the oocytes specifically accumulate vitellogenine from the haemolymph. The final stage is choriogenesis, in which the proteinaceous eggshell (chorion) is secreted around the oocyte. Follicular cells are responsible for controlling the access of proteins and nutrients to the oocytes for secretion of the chorion. The histology of the development of the ovaries of G. lacustris is synchronised, as similarly described in H. coagulata (Hummel et al. € 2006) and Graphosoma lineatum (Ozyurt et al. 2013). Our observation is that each ovary contains 4 ovarioles. The pedicel of the ovarioles in G. lacustris, opens into the apical bulb of their respective lateral oviducts. The walls of the pedicel and lateral oviduct in G. lacustris is surrounded by a single layer epithelium of cylindirical cells whereas in S. rusticum the pedicel is composed of simple cuboidal cells (Jawale & Ranade 1990), and in A. ovatus. the epithelial cell is squamous (Lalitha et al. 1997). The epithelial nuclei are ovoid in these species (Jawale & Ranade 1990; Lalitha et al. 1997). In G. lacustris as in S. rusticum, epithelial cells are enveloped by a layer of muscle (Jawale & Ranade 1990). In G. lacustris, as other Heteroptera, the common oviduct, also known as the median oviduct, is formed by the merging of the paired lateral oviducts. The common oviduct opens posteriorly into a genital chamber or vagina (Ma & Ramaswamy 1987; Jawale & Ranade 1990; Lalitha et al. 1997; Stys et al. 1998; Vogelsang & Szklarzewicz 2001; Lis 2003; de Paulo Lemos et al. 2005; Hummel € et al. 2006; Uceli et al. 2011; Ozyurt et al. 2013; Mattison et al. 2017). This study provides information on the female reproductive system histomorphology of G. lacustris. These findings will contribute to future studies on the diversity of the reproductive histomorphology in female Heteroptera. Acknowledgments We also thank Dr. Robert Lavigne (Professor Emeritus, University of Wyoming, Laramie, Wyoming, U.S.A.), who revised the grammar of this article.
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