ISSN 19950829, Inland Water Biology, 2015, Vol. 8, No. 2, pp. 113–120. © Pleiades Publishing, Ltd., 2015. Original Russian Text © J.V. Korneva, N.M. Pronin, 2015, published in Biologiya Vnutrennikh Vod, 2015, No. 2, pp. 14–22.
BIOLOGY, MORPHOLOGY, AND SYSTEMATICS OF HYDROBIONTS
Fine Structure of the Copulatory Apparatus of Nippotaenia mogurndae Yamaguti et Miyato, 1940 (Cestoda, Nippotaeniidea) J. V. Kornevaa and N. M. Proninb a
Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Nekouzskii raion, Yaroslavl oblast, 152742 Russia email:
[email protected] b Institute of General and Experimental Biology, Siberian Branch, Russian Academy of Sciences, ul. Sakhyanovoy 6, UlanUde, 670047 Russia Received December 20, 2013
Abstarct—The fine structure of the copulatory apparatus of Nippotaenia mogurndae Yamaguti et Miyato, 1940 has been studied by transmission electron microscopy. Structures of the cirrus sac and the genital atrium, the ultrastructural organization of genital ducts of the copulatory apparatus, and unicellular prostate glands localized in the cirrus sac have been described. On the surface of the atrium epithelium, tubular and conical microtriches are observed similar to tegumental microtriches. The absence of microtriches on the apical surface of the cirrus and vaginal epithelium and an increase in the number of layers of underlying mus culature in these ducts when compared to other sections of the copulatory apparatus have been determined. The conclusion about the possibility of cross fertilization due to the active movements of segments separated from the strobila with developed genital complexes and a nonformed uterus is based on the peculiarities of the copulatory apparatus structures, behavior, and biology of N. mogurndae. A comparative analysis of the copu latory apparatus peculiarities and their armaments in cestodes from different orders is discussed. Keywords: Cestoda, Nippotaenia mogurndae, reproductive system, copulatory apparatus, ultrastructure DOI: 10.1134/S1995082915020091
INTRODUCTION Works on the study of the reproductive system do not cover all orders of cestodes. Most studies on the ultrastructure of the copulatory apparatus and ducts of the reproductive system have been performed on rep resentatives of cestodes of the family Cyclophyllidea [5, 13–15, 17, 30, 32, 33, 39]. There are very few stud ies on the fine structure of other more primitive orders of cestodes—representatives of the orders Caryophyl lidea [6, 7, 25], Spathebothriidea [26, 38] and Proteo cephalidea [10, 16, 36]. There are also data on several species which are presently related to the orders Both riocephallidea [12, 24, 37] and Diphyllobothriidea [22, 23]. The order Nippotaeniidea is peculiar cestodes whose scolex is an apical sucker that captures a region of the host intestine and restrains it due to the strong contraction of its circular sphincter (Fig. 1a). A sin gle family, including one genus comprised of two spe cies, makes up the order. The study of ultrastructural organization of certain parts of the reproductive sys tem and the uterus formation in Nippotaenia mogurndae were started earlier by V.G. Davydov and Zh.V. Korneva [11, 31].
The aim of present work is to study the fine struc ture of the male and female copulatory apparatus in N. mogurndae for a comparative analysis of the repro ductive system ultrastructure in cestodes of different taxa and identifying the main paths it develops. MATERIALS AND METHODS Nippotaenia mogurndae Yamaguti et Miyato, 1940 (Cestoda, Nippotaeniidea) were collected from the intestine of the Chinese sleeper Perccottus glenii Dybowski, 1877, caught in Lake Karasinoe in the Selenga River valley (Ivolginsk raion of the Buryat Republic), because the sleeper has spread throughout the Baikal region as an introduced species [27, 28]. Parasites and mature segments separated from the strobila were fixed. For transmission electron microscopy studies, fix ation was carried out in 2.5% glutaraldehyde in a cacodylate buffer (pH 7.4); then the specimens were postfixed with 1% osmium tetroxide in the same buffer and dehydrated in a graded ethanolacetone series. During dehydration, the material was stained for 12 h in 1% uranyl acetate in 70% ethanol. Then the specimens were impregnated with epoxy resin,
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Cirrus Sac
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Mt
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Fig. 1. Schematic representation of Nippotaenia mogurndae: (a) total view of a parasite and (b) copulatory apparatus; (A) lumen of the genital atrium, (V) vaginal cavity, (M) muscular layers, (Mc) muscle cells, (Mt) microtriches, (P) prostate gland, (ED) ejaculatory duct, (SV) seminal vesicle, and (C) cirrus.
embedded in araldite, and polymerized for 1 day at 36°C and 2 days at 60°C. Ultrathin sections (60– 90 nm thick) were made on ultramicrotome Leica and placed on grids, stained in Reynolds lead, and observed in a JEM–1011 transmission electron micro scope. The identification of the reproductive system sections was done on semithin sections stained in 1% toluydine blue. RESULTS The copulatory apparatus of Nippotaenia mogurndae consists of a cirrus sac, vagina, and genital atrium (Fig. 1b), which are completely formed in the last segment of the attached parasite and in separated segments, which actively move in the host intestine similar to independent organisms.
The cirrus sac of N. mogurndae is confined outside by four–five layers of variously oriented muscle fibers. Between the ejaculatory duct and outer muscle wall of the cirrus sac, there are small muscle fibers with con tractile fibrils related to separate muscle cells from which numerous thickened cytoplasmic outgrowths deviate. Moreover, outgrowths, filling the cirrus sac, are formed by the muscle cells of the circular muscu lature of the ejaculatory duct and outer muscular layer of the cirrus sac. These outgrowths are positioned par allel to each other, forming thick stacks; they contain neither myofibrils nor cellular organoids; in their cyto plasm, cytoskeleton elements are mainly observed. Lipid inclusions are collected in the cytoplasm of muscle outgrowths (Figs. 2a, 2b). In the entry of the cirrus sac, the spermaduct wid ens and forms a small seminal vesicle in which wall enlarged cisterns of the granular endoplasmic reticu lum (GER) are observed. The muscular layer sur rounding the seminal vesicle becomes thicker than in the spermaduct and attaches to the basal matrix with numerous hemidesmosomes, which allows seminal ves icle to contract and the portioned exit of spermatozoa. Cells of prostate glands in the cirrus sac are not numerous; however, depending on the functional con dition in these cells, active synthetic processes and welldeveloped GER (the enlarged cisterns of which can reach 2 µm in length and 1 µm in width) can be observed. Outgrowths of prostate glands are filled with small electrondense secretory granules of round or rodlike form (up to 0.4 µm). Terminal sections of glan dular ducts are strengthened with microtubules on the periphery. Most exits of prostategland secretions are localized in the distal part of the ejaculatory duct and in the proximal part of the cirrus, which differ insignif icantly (Figs. 2a, 2c–2d). The ejaculatory duct is confined outside by the basal matrix and one–two layers of the circular mus culature, which attach to the matrix with hemides mosomes. The epithelium of the ejaculatory duct is different morphologically along the whole length (Figs. 2d–2f, 3a–3c). In the proximal part, the epi thelium does not have long and branched folds with thickenings on the ends on its surface (Figs. 2e, 3a). In the cytoplasm, there are nuclei and vacuoles are not numerous. In the middle part of the ejaculatory duct, the epithelium looks strongly vacuolated and cut by invaginations. On its surface there are numerous lamellae having different thicknesses and connected with each other by anastomoses. Nuclei are localized either in the thickness of the epithelial layer or in the lumen of a canal, connecting with the epithelial layer by cytoplasmic “bridges” (Figs. 2d, 3b). Close to the distal part, secret exits of prostate glands become sin gular. The thickness of the circular musculature layer, and also the thickness and vacuolization of the epithe lial layer increase (Figs. 2f, 3c (left)). INLAND WATER BIOLOGY
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Fig. 2. Male copulatory apparatus of Nippotaenia mogurndae (transmission electron microscope): (a) cirrus sac, filled with stacks of outgrowths of muscle cells (indicated as arrows) and cells of prostate glands (indicated as a double arrow); (b) outer muscular layer of the cirrus sac (indicated as arrow) confining it from surrounding tissues; (c) cells of the prostate gland in the cirrus sac; (d) duct of the prostate gland (indicated as arrow) in the middle part of the ejaculatory duct; (e, f) proximal and distal parts of the ejaculatory duct, respectively; (g) cirrus (insert: group of basal invaginations in the cirrus epithelium); (L) lipids, (E) epithelium of the genital duct, (ER) endoplasmic reticulum, and (N) nucleus. The rest of the designations are the same as in Figs. 1 and 2.
Ultrastructurally the cirrus does not differ from the proximal part of ejaculatory duct. On the apical sur face of the epithelium, microtroches are absent, lamellae shorten and thicken, and the epithelial layer is strongly vacuolated (Fig. 2g). In the proximal part of the cirrus there are not numerous exits of prostate glands. On the basal surface of the epithelial layer there are thin invaginations, sometimes located paral INLAND WATER BIOLOGY
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lel to each other at equal distance and reaching 2.5 µm (Figs. 2g, 3c (right)). Vagina On the apical surface of the vaginal epithelium of N. mogurndae, like in the cirrus, there are numerous long outgrowths and no microtriches. The female gen
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Fig. 3. Scheme of the ejaculatory duct structure and the cirrus of Nippotaenia mogurndae: (a, b) epithelium of the proximal and middle part of the ejaculatory duct, respectively; and (c) epithelium of the distal part of ejaculatory duct (left) and cirrus (right). The basal matrix is indicated as arrows. The rest of the designations are the same as in Figs. 1 and 2.
ital duct is surrounded by several layers of variously oriented muscle fibers (Fig. 4a). The epithelium, underlying the duct, in the thickness of a layer con tains nuclei and can reach 8 µm in these parts (Fig. 4b). Separate nuclei evaginate in the duct lumen, connecting with the epithelium by cytoplasmic out growths. In the distal part the thickness of the epithe lial layer increases and reaches 10–12 µm. The epithe lium is penetrated with narrow invaginations, starting on the apical surface and reaching almost the basal side (Fig. 4a), where the epithelium underlies a thin distinct layer of the basal matrix. In its distal part (in immediate proximity to the genital atrium) vagina is surrounded by strong muscular lining from 5–7 vari ously oriented layers.
Genital Atrium The epithelium of atrium is identical to the tegu ment and bears on its apical part microtriches of two types (Fig. 4c). The first type are typical filamentous microtriches with a long and thin basal part (up to 1.5 µm) and with the same length and a thin apical part (up to 2.8 µm). The second type of microtriches are bladelike with strong basal and apical parts, reaching 1.3 and 2.5 µm in length, respectively (Fig. 4c (insert)). DISCUSSION A collection of new knowledge on the fine structure of different specialized systems in cestodes allows con INLAND WATER BIOLOGY
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E M
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Fig. 4. Female copulatory apparatus of Nippotaenia mogurndae (transmission electron microscope): (a) muscular layers underly ing the vaginal duct, penetrated by numerous invaginations (indicated as arrows); (b) nuclear area of the vaginal epithelium; and (c) genital atrium (insert: two types of microtriches on the apical surface of the atrium epithelium). The rest of the designations are the same as in Figs. 1 and 2.
sidering a variety of forms appearing on a common morphological basis. The reproductive system, whose polyvariant development comprises one of the pecu liar features in flatworms, deserves special attention. The cirrus sac, described in N. mogurndae, has a structure similar to the copulatory apparatus of many ultrastructurally studied “lower” cestodes [12, 16, 22–25, 29]. In a more typical case, the cirrus sac is confined from parenchyma by several layers of muscle fibers; it contains circular fibers of the musculature, an underlying epithelium of the genital duct, thin cyto plasmic outgrowths of muscle and neurosecretory cells, and in some species of cestodes there are cells of prostate glands. A peculiar cirrus sac is described in INLAND WATER BIOLOGY
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Caryophyllaeus laticeps (Pallas, 1781) (Caryophyl lidea); it is formed by variously oriented muscle fibers not separating into any layers [6]; in Phyllobothrium vagans Haswell, 1902 (Tetraphyllidea) the cirrus sac contains muscle and neurosecretory cells and is con fined from parenchyma by a single layer of flattened cells with numerous mitochondria, lipid droplets, and a filamentous outgrowth [30]. In higher cestodes the layer of basal matrix appears together with muscular layers, confining the cirrus sac from the surrounding parenchyma [14, 15, 17, 32, 39], while in Sobolevican thus gracilis (Zeder, 1803) the cirrus sac is confined by two thin muscular layers and hypertrophied fibrous
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connective tissue matrix, whose thickness reaches 2.5 µm [5]. In their localization, origin, and probably func tional importance, prostate glands demonstrate numerous variants, which in their own diversity are observed in different orders of cestodes. Prostate glands of Nippotaenia mogurndae, as in the majority of flatworms, are presented by unicellular glands local ized inside the cirrus sac. The gland ducts are armored with microtubules and connected with the epithelium of the ejaculatory duct with septate desmosomes [2, 10, 23, 35, 40]. If prostate glands are localized out side the cirrus sac, glandular cells and their ducts are localized in parenchyma surrounding the cirrus sac and open either into spermaduct [24, 33] or in the ejaculatory duct [7]. In Diphyllobothrium latum (L.), prostate glands are found both in and out of the cirrus sac, but the gland ducts open into the median part of the spermaduct [26]. However, there are known spe cies related to different orders of cestodes in which prostate glands are absent [10, 14, 15, 17]. Among all studied flatworms, two cases are described when glan dular cytons localized in the cirrus sac are connected with the cirrus epithelium (in trematode Maritrema linguilla Jagerskiold, 1908) [35] and with the epithe lium of inner bursal part of the spermaduct (in cestode Sobolevicanthus gracilis) by cytoplasmic bridges (but nonspecialized ducts with septate contacts) [5]. In these species, morphofunctional modifications of the epithelium of genital ducts and the formation of spe cific prostate glands are observed. The condition of small parts of the syncytial layer having the ability to synthesize secretory vesicles different in structure and functions [2, 4] is typical for flatworms. A complex genital system characterized by internal fertilization and having a system of special excretory ducts appears in lower worms for the first time and demonstrates a wide specter of different structural decisions [1], which is also true in relation to prostate glands in which the diversity of forms and different localization are observed. Because the presence and peculiarities of develop ment of prostate glands vary within all studied orders of cestodes, these factors are not connected with the height of level of parasite organization. It is possible to assume that the functioning of prostate glands is con nected with fertility, which directly depends on the peculiarities of cestode life cycles, as is shown in hymenolipid cestodes [3]. In trematodes, prostate glands are mainly described inside the cirrus sac; however, there are known species with glands outside the sac [2, 35, 42]. Prostate glands of two and three types are described in some species of trematodes, while such differences are observed even in species related to one genus Prostho dendrium [21]. In Allassogonoporus amphoraeformis (Modlinger, 1930) lacking the cirrus sac, one type of glands opens in the seminal vesicle and another in the ejaculatory duct [20]. It is observed that the secret
excretion and the passage of sperm though the ejacu latory duct occurs synchronically [34]. There are different assumptions about possible functions of prostate glands: the stimulation of sper matozoa, previously being at the dormant stage in the seminal vesicle; the energy supply of the sperm in addition to glycogen; and the effect on female repro ductive ducts and their stimulation [40]. In the opin ion of other researches [7, 23], the gland secret sur rounds spermatozoa and facilitates copulation or per forms a protective function and promotes their movement through the spermaduct. In some animals, the discharge produced by prostate glands contains immunoglobulins, ferments, vitamins, lemon acid, zinc ions, etc. It participates in the liquefaction of ejaculate; moreover, at the result of fructose collapse contained in the discharge, the energy needed for acti vation and vital functions of spermatozoa is released. The discharge of prostate glands found in flatworms probably functions similarly. The absence of prostate glands in some cestodes, as well as the presence of one, two, or even three types of discharge, is evidence that the structure is under formation; thus, in different spe cies it is possible to see the specter of morphofunc tional conditions characteristic for animals with low level of organization [9, 18, 19]. Microtriches on the surface of copulatory ducts, which differ in structure and diversity of morphologi cal types, are described in most studied cestodes from different orders [6, 15, 17, 25, 26, 30, 32, 36, 38, 39]. The characteristic peculiarity for Nippotaenia mogurndae is the absence of any microstructures on the apical surface of the cirrus and vagina. A similar feature is also characteristic for Eubothrium rugosum (Batsch, 1786): the only cestode for which the absence of microtriches on the surface of copulatory ducts is revealed [24]. This character is explained by the local ization and high intensity of invasion, because para sites attach in pyloric appendages of the burbot by “dense strands” and hang down into the intestinal lumen that promotes the process of cross mating [24]. By autoradiography it has been shown that if in one host there are several individuals of cestodes, their selffertilization occurs in exceptional cases [8]. For Nippotaenia mogurndae, selffertilization is an extremely doubtful process, because a cestode has one–two mature hermaphrodite segments and short copulatory ducts, lacking microtriches, located very close and opening into the common genital atrium. The invasion intensity of the Chinese sleeper (a host of N. mogurndae) is high (index of abundance up to 60.7 specimens) [29], which makes the cross copula tion of parasites more expected. Moreover, last seg ments of N. mogurndae are capable of rejection, and not only segments with a uterus filled with eggs sepa rate from the strobila, but also segments with devel oped genital complexes and an incompletely formed uterus. As separated segments are able to move actively and function as independent organisms, it is possible INLAND WATER BIOLOGY
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to assume that segments with formed genital apparatus and undeveloped uterus enter the process of cross cop ulation between each other or with attached parasites. The absence of microtriches on the surface of the cir rus sac and vagina in the present process can be com pensated for by the developed musculature of the cir rus sac and the vaginal duct of N. mogurndae. This is especially brightly reflected in the structure of the vagina, confined by 5–7 layers of the musculature, while for N. mogurndae the weak development of the circular musculature is characteristic, providing the peristaltic contraction of other ducts of the reproductive system and the advancement of genital cells [11]. In Acanthobothrium quadripartitum Williams, 1968 (Tetraphyllidea), large distal spines restrain the vaginal epithelium during copulation, which allows the dipper to enter the cirrus [41]. According to Jones [32], the position of spines and large microtriches in the distal part of the cirrus is explained by their active participa tion in copulation, which provides a closer contact of reproductive structures. The cases of simultaneous development of surface microstructures and the mus cular lining have been noted. For example, in Cyatho cephalus truncatus Pallas, 1781, the outer wall of the cirrus sac is confined by 20 layers of muscle fibers and on the surface of the cirrus epithelium strong cone shaped microtriches are present [38], while the para site localizes in pyloric appendages of the fish intes tine, like for Eubothrium rugosum, for which the absence of microtriches on the surface of copulatory ducts is characteristic [24]. Thus, the presence or absence of microtriches in the genital ducts of the cop ulatory apparatus is caused not only by the localization of parasites, but also by peculiarities of copulation. CONCLUSIONS The peculiarities of the copulatory apparatus struc ture in Nippotaenia mogurndae appeared in many characteristics similar to the reproductive apparatus of other lower cestodes, first and foremost, from the order Proteocephalidea. One specific distinction of the structure of Nippotaenia mogurndae copulatory apparatus is the absence of microtriches on the surface of the cirrus and vagina, which participate in the cop ulation of cestodes. This peculiarity of the structure is compensated for by the intensive motor activity of seg ments separated from the strobila that can participate in cross mating. REFERENCES 1. Beklemishev, V.N., Osnovy sravnitel’noi anatomii bespozvonochnykh (Fundamentals of Comparative Anatomy of Invertebrates), Vol. 2: Organologiya (Orga nology), Moscow: Nauka, 1964. 2. Galaktionov, K.V. and Dobrovol’skii, A.A., Germa froditnoe pokolenie trematod (Hermaphroditic Genera tion of Trematodes), Leningrad: Nauka, 1987. INLAND WATER BIOLOGY
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Translated by E. Guzeeva
INLAND WATER BIOLOGY
Vol. 8
No. 2
2015
