Structure of the Ovaries in Larvae and Mature Females of Euholognathan

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BlackwellStructure Science, Ltd of the ovaries in larvae and mature females of euholognathan stoneﬂies (Plecoptera) Elzbieta Rosciszewska

Abstract Department of Systematic Zoology, Rosciszewska, E. 2001. Structure of the ovaries in larvae and mature females Institute of Zoology, Jagiellonian, of euholognathan stoneflies (Plecoptera). — Acta Zoologica (Stockholm) 82: University, R. Ingardena 6, PL-30–060 307–314 Kraków, Poland The morphology of ovaries, oviducts and egg capsules in four species of Keywords: euholognathan stoneflies was investigated. The characteristic features found oogenesis, panoistic ovariole, “nuage”, were as follows: (i) numerous, long ovarioles, that open individually to the eggshells extensively folded, lateral oviducts; (ii) a thin, morphologically undifferentiated chorion; (iii) a thick gelatinous layer (extrachorion) which acts as an adhesive Accepted for publication: layer fixing the eggs to the substrate. Additionally, in the larval ovariole of Leuctra 6 February 2001 sp. the terminal filament anlage and clusters of germ cells have been found. These observations are in agreement with the classification of stonefly ovaries as primary (true) panoistic. Elzbieta Rosciszewska, Institute of Zoology, Jagiellonian University, R. Ingardena 6, PL-30–060 Kraków, Poland. E-mail: [email protected]

taxonomy of the order (Lillehammer and Økland 1987; Introduction Stark and Szczytko 1984). Similar morphological features Stoneflies (Plecoptera) are ancient (known since early Perm) have been successfully used as additional taxonomic traits in and relatively primitive insects (for reviews see: Hennig Ephemeroptera (mayflies) (Gaino et al. 1987, 1989; Gaino 1981; Sinitschenkova 1997; Zwick 2000). The phylogenetic and Mazzini 1988; Mazzini and Gaino 1990; Gaino and relationships between plecopterans and other insect orders Bongiovanni 1992, 1993). As pointed out by Sivec et al. are still not clear (Zwick 2000). It has been recently shown (1988) and Stark and Szczytko (1988a), the egg capsule that the morphology of internal organs constitutes a good morphology may help in resolving stonefly phylogenetic character for inferring phylogenetic relationships. Stys and relationships, as was demonstrated in the case of mayflies Bilinski (1990) have suggested that ovaries are particularly (Degrange 1960; Koss and Edmunds 1974; Klonowska- useful for such analyses. In stoneflies the morphology of Olejnik 1997). Ultrastructural studies of ovary and oogenesis ovaries, as well as the process of oogenesis, have been only in Plecoptera belonging to Euholognatha were until now partially characterized. Some ultrastructural investigations relatively rare (Gottanka and Büning 1990; Rosciszewska have been done on species of the systellognathan group 1996b). Here, the results of studies focusing on the structure (Zwick 1973; Kis 1974). More recently, the structure of the of the ovaries in both larvae and adults of the euholog- larval and mature ovaries (Rosciszewska 1989, 1997) and the nathan stoneflies are presented. process of chorion formation (Rosciszewska 1995, 1996a) have been described. In addition, the structure of the accessory Materials and Methods ovaries found in males of some Perlidae species has been investigated (Rosciszewska and Soldàn 1999). There are The adults and larvae of four stonefly species were collected also several scanning and transmission electron micro- close to springs, or streams and small river banks in several scope (SEM and TEM) studies on the eggshells (Stark mountainous regions of southern Poland. The species represent and Szczytko 1982, 1984, 1988b; Stark 1986; Rosciszewska three families belonging to the arctoperlarian group – 1991a, 1991b; Rosciszewska and Jankowska 1993; Isobe Euholognatha: Brachyptera risi (Morton, 1896) ( Taeniopterygidae), 1997). The external features of the plecopteran egg capsules Protonemura auberti Illies, 1954 (Nemouridae), Leuctra nigra seem to be species-specific and thus can be useful in the (Olivier 1811) and Leuctra autumnalis Aubert, 1948 ( Leuctridae).

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The mature females were collected during their egg laying open individually into the lateral oviduct (LO) (Fig. 1A,B). periods, in the following localities: P. auberti and L. nigra – Góry In older females the LOs are filled with numerous eggs. In Stolowe, the Sudety Mountains, May 1998; B. risi – the Jaszcze Protonemura auberti in each cross-section through the LO as stream Valley near Ochotnica Górna, the Carpathian Gorce many as eight eggs were present. The ovarioles are surrounded Mountains, June/July 1999; L. autumnalis – the Wetlinka river by a network of tracheae and they are in close contact with Valley near Wetlina, the Bieszczady Mountains, August 1996, the lobes of the fat body (Fig. 1A). In the posterior part of the 1998. The larvae of Leuctra sp. were found in the river abdomen, the LOs fuse to form an unpaired common oviduct. Wetlinka, in October 1998. The anterior ends of the LOs also fuse (not shown). The only The ovaries, dissected from adults and larvae, and eggs, exception to this rule was found in Leuctra, where the anterior extracted from the mature females’ oviducts, were examined ends of the LOs remain separated. In contrast to Leuctra and by light microscopy (LM), and both SEM and TEM. Protonemura, in Brachyptera risi LOs are extensively folded For the LM the ovarioles were dissected and fixed in and covered with a layer of muscle. 4% paraformaldehyde in phosphate-buffered saline (PBS) and analysed using the Nomarski contrast, or fixed as for The ovariole TEM (see below). Semi-thin epon sections (1.5 µm) were stained with 1% methylene blue in 1% borax (Litwin 1985) The ovarioles of all investigated species are panoistic. and examined using a Jenalumar Carl Zeiss Jena light They are composed of short, anteriorly located germaria and microscope. the posterior vitellaria. Degenerating cells have never been observed in the germaria. Each vitellarium houses about 20 ovarian follicles. The follicles are linearly arranged, in Electron microscopy consecutive stages of oogenesis (Fig. 1B,D). The wall of the For SEM studies the ovaries and eggs were fixed in 2.5% ovariole consists of the thick basal lamina – tunica propria glutaraldehyde in 0.1  phosphate buffer, pH 7.4, for 72 h. (Figs 1B, 2D). Haemocytes are often seen in close contact Then they were rinsed several times in phosphate buffer, with the basal lamina. The outer ovariolar sheath – the pH 7.4, containing 5.8% sucrose and fixed for 2 h with 1% tunica externa – has never been observed. The characteristic

OsO4 in 0.1  phosphate buffer, pH 7.4. The specimens were feature of the adult ovarioles in all the species studied is the rinsed several times in water, dehydrated in a graded series lack of the terminal ﬁlaments (Fig. 1B).

of acetone, critical point dried using liquid CO2 and coated with gold. They were examined with a Jeol JSM-5410 SEM The oocytes at 25 kV. For TEM studies, the specimens fixed as described above Previtellogenic oocytes are located in the anterior part of the were dehydrated in a graded series of ethanol and acetone vitellarium, i.e. next to the germarium (Figs 1B,D, 2D). The and embedded in Epon 812. Sections were cut with a Reichert oocyte nuclei are spherical and contain prominent nucleoli ultramicrotome. Ultrathin sections, contrasted with uranyl (Figs 1D, 2D,E). Numerous pores perforate the nuclear acetate and lead citrate were examined in a Phillips 300 electron envelope (Fig. 2D,E). In the ooplasm of the youngest oocytes microscope at 60 kV. accumulations of mitochondria and vacuoles filled with an electron-dense material are present. There are two types of ‘nuage’ material in the perinuclear cytoplasm. The first consists Results of electron-transparent material in which electron-dense grains occur. The second type has a form of irregular electron- Gross architecture of adult ovaries dense accumulations immersed in the nuage of the first type The mature ovaries of the investigated species are paired. (Fig. 2D,E). The cytoplasm of the growing previtellogenic Each ovary is composed of numerous long ovarioles that oocytes when stained with methylene blue reveals dark and

Fig. 1 —A. SEM, fragments of the ovary of the mature female of auberti. The surface is morphologically undifferentiated (with Brachyptera risi. Note numerous, long ovarioles (ov), a thick lateral the exception of very small micropylar openings – arrows). oviduct (white arrow) consisting of two layers: a deeply folded Bar = 20 µm. —D. LM, methylene blue, a semi-thin, longitudinal oviductal epithelium surrounded by a layer of muscles. The apices of section of an ovariole of Leuctra nigra. The ovarian follicles (each the ovarioles are devoid of terminal ﬁlaments. The tracheae (white consisting of an oocyte (o) enveloped by a single layer of follicular arrowhead) and fat body (asterisk) associated with the ovary are seen cells (asterisk) in consecutive stages of oogenesis. In the previtellogenic (most of the tracheae and fat body have been removed). Bar = 100 µm. oocyte bright and dark cytoplasm can be seen; the voluminous —B. LM, Nomarski contrast. A whole mount of the ovariole of nucleus contains a prominent nucleolus (arrowhead); precursors Protonemura auberti. Note lack of terminal ﬁlament, a short of vitelline envelope (thick arrow) are seen in the peri-oocytic space. germarium (g) and a long vitellarium (v) housing numerous growing The vitelline envelope deposited on older oocytes surfaces (medium oocytes (o). Bar = 20 µm. —C. SEM, the egg capsule of Protonemura and late vitellogenesis stages) can be observed. Bar = 20 µm.

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bright regions (Fig. 1D). At the ultrastructural level the dark germ cells, a short vitellarium and a terminal filament anlage. cytoplasm corresponds to electron-dense areas rich in ribo- The terminal filament anlage consists of two to eight flattened somes while the bright regions correspond to the electron- somatic cells arranged in a stack at the tip of the germarium transparent areas that contain mainly cisternae and vesicles (Fig. 2A,C). During further development the terminal fila- of the rough endoplasmic reticulum (RER), mitochondria ment anlage degenerates and consequently this structure is and occasionally dictyosomes (not shown). not observed in adult ovarioles (compare previous paragraph). The oocytes are surrounded by an opaque layer of the In the germarium clusters of germ cells (oogonia, oocytes) vitelline envelope (VE) precursors (Fig. 1D) and a single- connected by intercellular bridges as well as single somatic layered follicular epithelium. Follicular cells are cube-shaped cells (Fig. 2B) are present. The large, spherical nuclei of the and contain large spherical nuclei with prominent nucleoli. oocytes contain prominent nucleoli (Fig. 2A,B). In the The posterior part of the vitellarium is occupied by oocytes perinuclear cytoplasm, two types of nuage material, morpho- in consecutive stages of vitellogenesis. In the peri-oocytic space logically similar to nuage types observed in the adult ovarioles, of the vitellogenic oocyte, the VE is clearly visible (Fig. 1D). are encountered (Fig. 2B). Numerous mitochondria accu- The oldest (and largest) oocytes in the ovarioles, i.e. the terminal mulated around ER vesicles are also present in the ooplasm oocytes, are densely packed with yolk plates and lipid droplets (Fig. 2B). Within the vitellarium, a few successfully developing (Fig. 1D). A comparatively thick VE is deposited on their ovarian follicles are found. Each follicle consists of an early surface (Fig. 1D). After completion of choriogenesis the previtellogenic oocyte, surrounded by a single-layered follicular synchronously developing terminal oocytes, covered with the epithelium (Fig. 2A, asterisk). The oocyte contains the volu- fully formed egg capsules, are transferred to the LOs. minous, spherical nucleus equipped with a large nucleolus. In the ooplasm, nuage accumulations as well as numerous organelles are present (not shown). The eggs The eggs dissected from the oviducts were analysed by SEM. Discussion The shapes of the eggs are variable. In Protonemura auberti (Nemouridae) the eggs are spherical (Fig. 1C); in Leuctra Gross architecture of the gonad nigra and in L. autumnalis (Leuctridae) they are oval; in Brachyptera risi (Taeniopterygidae) the eggs are polyhedral. The typical insect ovary is a paired structure that comprises The external surface of the egg capsules does not show any a bundle of ovarioles connected with the lateral oviduct (LO). regional specializations except for very narrow micropylar LOs join together to form a common oviduct ( King and Büning openings (Fig. 1C). The radial organization of the investi- 1985). The organization of ovaries in euholognathan stone- gated egg capsules is simple. They are composed of a vitelline flies, as well as in Systellognatha, does not precisely follow envelope, a thin, double-layered chorion (not shown) the described scheme. One can find more similarities with and extrachorion, which serves as an adhesive layer. After Myriapoda. As in Scolopendra (Klapálek 1896; Matsuda 1976), deposition, in water, it swells and becomes sticky so as to both the anterior and the posterior ends of the oviducts are firmly attach the egg to the substrate. A detailed ultrastructural joined. As a result, a characteristic oviduct ring is formed study of the egg capsule and choriogenesis of Leuctra autumnalis (Zwick 1973; Matsuda 1976; Rosciszewska 1989, 1997; will be presented in a separate paper (Poprawa et al. in Büning 1994; and this paper). Exceptions to this rule were preparation). only found in representatives of Leuctridae and Capniidae (Klapálek 1896; Zwick 1973; Matsuda 1976). Moreover, the ovarioles in Plecoptera do not form bundles, but instead The larval ovariole are arranged circumferentially along the LO and each opens The ovariole of the Leuctra sp. larva is spindle-shaped, enveloped individually into the LO (Büning 1994; Matsuda 1976; by a basal lamina (tunica propria) and composed of three Rosciszewska 1989, 1997). A similar arrangement of the regions: a relatively long germarium filled with numerous ovarioles was reported in only a few insects (Soldàn 1979a,b;

Fig. 2—A. LM, methylene blue. A longitudinal semi-thin section cells. Bar = 2 µm. —D. TEM, longitudinal section through the through the larval ovariole of Leuctra sp. Note squamous somatic upper part of the vitellarium of the ovariole of the mature female cells of the terminal filament anlage (t), the germarium (g) filled of Leuctra autumnalis. Note a large oocyte nucleus with prominent with young oocytes and a fragment of the vitellarium (v). Asterisk – nucleolus as well as ‘nuage’ material (*, **) in perinuclear space and follicular cell. Bar = 20 µm. —B. TEM, as Fig. 2(A), ultrathin the accumulation of organelles (arrows). Bar = 2 µm. —E. TEM, section. A fragment of the germarium. The intercellular bridge (b) as Fig. 2(D). A fragment of an oocyte, representing a part of the is connecting the oocytes. two types of ‘nuage’ materials (*, **) and electron-dense nucleolus in close contact with a cloud of fibrillar accumulations of the organelles (arrows) can be recognized in the material (arrowheads). Several pores (arrows) perforating the ooplasm. Bar = 2 µm. —C. TEM, a fragment of Fig. 2(A), enlarged. nuclear envelope as well as two types of ‘nuage’ (*, **) are visible. The terminal filament anlage (t) consists of several flattened somatic Bar = 1 µm.

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Gaino and Mazzini 1990; Bilinski and Szklarzewicz 1992; Previtellogenesis Bilinski 1994). In the investigated euholognathan species numerous eggs EM investigations on Leuctra ovaries revealed the abundance fill the LOs. In one of the species, namely Brachyptera risi, of nuage material (see: Eddy 1975; Klag and Ostachowska- eggs were polyhedral thus allowing for very tight packing Ga¸sior 1997 for a review) around the oocyte nucleus during without empty spaces between eggs. In this species the lateral previtellogenesis. This observation, as well as the presence of oviducts, prior to filling with the eggs, show extensive folding. a large nucleolus, suggests a high metabolic activity of pre- It seems that such an organization allows for a substantial vitellogenic oocytes. expansion and subsequent accommodation of very large num- In the investigated stonefly ovaries, secretion of eggshells bers of eggs. Similar oviducts were found in Thaumatoperla starts relatively early. Similarly, early deposition of egg envelopes flaveola (Rosciszewska, unpublished) a species belonging to has been described in myriapods, crustaceans and arachnids the stonefly subgroup, Antarctoperlaria: Eustheniidae (Zwick (Nørrevang 1972; Herbaut 1974; Witalinski and Zuwala 1973, 2000; Hennig 1981). According to Hinton (1981), 1981; Witalinski 1993; Ikuta et al. 1997). The comparison of Thaumatoperla flaveola can lay up to one thousand eggs at choriogenesis in the Euholognatha and the Systellognatha one time. Similarly, females of several euholognathan suggest an early onset of chorion formation is a plesiomorphic species lay numerous eggs, which considerably raises the character of Plecoptera. chances of reproductive success. The species with embryos that undergo a diapause, for example Podmosta macdunnoughi Acknowledgements (Harper et al. 1993), have still better chances, especially when the conditions in the aquatic habitat undergo a drastic I would like to express my gratitude to Professor Dr P. Zwick worsening. and Professor Dr S.M. Bilinski for critical reading of the manuscript and for their valuable comments. I am grateful to Dr M. Jaglarz for his suggestions. I acknowledge the kind The ovarioles help of Professor Dr W. Kilarski who provided the access to Ovarioles in adult females of the Euholognatha (Zwick 1973; SEM facilities in his laboratory and to Dr J. Faber for profes- Gottanka and Büning 1990; and this study) are of the panoistic sional assistance. Thanks are also due to M.Sc. W. Jankowska type, similar to those found in Systellognatha (Rosciszewska and Dr B. Szymanska for excellent technical assistance 1989, 1997). However, in the larval germarium of Nemoura and to Dr W. Fialkowski for taxonomic expertise. This sp. (Euholognatha) (Gottanka and Büning 1990) as well as in study was supported by the Jagiellonian University Research Leuctra sp. (this study), and in Perla marginata (Systellognatha) Grant BW/27/IZ/2000 and also, in part by the Program (Rosciszewska 1997), clusters of germ cells, characteristic of SUBIN 94. meroistic ovaries were discovered. The presence of such clusters undoubtedly represents an advanced character and References has been interpreted by Gottanka and Büning (1990) as ‘a first step towards the meroism’. The present and earlier investiga- Bilinski, S. 1994. The ovary of Entognatha. In Büning, J. (Ed.): The tion on the plecopteran ovaries revealed some important Insect Ovary. Ultrastructure, Previtellogenic Growth and Evolution, differences between the structure of ovarioles in the euholo- pp. 7–30. Chapman & Hall, London. gnathan and systellognathan stoneflies. These are as follows: Bilinski, S. M. and Szklarzewicz, T. 1992. The ovary of Catajapyx aquilonaris (Insecta, Entognatha): ultrastructure of germarium and i Ovarioles of euholognathan stoneflies are long and consist terminal filament. – Zoomorphology 112: 247–251. of more than 20 oocytes while those in Systellognatha are Büning, J. 1994. Mesodermal tissues of the ovary. In Büning, J. (Ed.): much shorter and contain only three or four oocytes The Insect Ovary, Ultrastructure, Previtellogenic Growth and evolution, (Rosciszewska 1989, 1997). pp. 40–92. Chapman & Hall, London. ii In contrast to Systellognatha the germaria in Euholognatha Eddy, E. M. 1975. Germ plasm and the differentiation of the germ lack degenerating cells (Rosciszewska 1989). cell line. – International Review of Cytology 43: 229–280. Degrange, C. 1960. Recherches sur la réproduction des Ephéméroptercs. iii In the ovariole of Systellognatha the terminal filaments – Travaux Du Laboratoire d’Hydrobiologie et Pisciculture de l’Univer- are absent both in larvae and adults (Rosciszewska 1989, 1997). sité de Grenoble 50/51: 7–193. The same holds true for the ligament fixing the ovary in the Gaino, E. and Bongiovanni, E. 1992. Comparative morphology of body cavity (for reviews of a structure and function of terminal epithemata (polar chorionic structures) in the eggs of Ephemerella filaments see Szklarzewicz 1987; Kaulenas 1992; Büning ignita (Ephemeroptera: Ephemerellidae). – Transactions of the 1994; Lupa et al. 1999). In contrast, in the larval ovariole of American Microscopical Society 111: 255–265. Leuctra sp. a terminal filament anlage has been discovered. In Gaino, E. and Bongiovanni, E. 1993. Scanning electron microscopy of the eggs of Palingenia longicauda Olivier (Ephemeroptera, adult specimens of Leuctra the terminal filaments are absent. Palingeniidae). – International Journal of Insect Morphology and The fate of this structure throughout larval development has Embryology 22: 41–48. not been traced, however, it is obvious that it degenerates Gaino, E. and Mazzini, M. 1988. The fine structure of the chorionic during transition for larva to adult. projections of the Rhithrogena kimminsi Thomas (Ephemeroptera,

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Ovary structure in euholognathan stoneﬂies • Ros´ciszewska Acta Zoologica (Stockholm) 82: 307–314 (October 2001)

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