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ISSN 1063-0740, Russian Journal of Marine Biology, 2017, Vol. 43, No. 1, pp. 49–56. © Pleiades Publishing, Ltd., 2017. Original Russian Text © E.M. Skorobrekhova, V.P. Nikishin, 2017, published in Biologiya Morya.

ORIGINAL PAPERS Parasitology

The Morphological Peculiarities of the Acanthocephalan Corynosoma strumosum (Rudolphi, 1802) (Polymorphidae) in Paratenic Hosts, the Eelpout Zoarces elongatus (Kner, 1868) (Zoarcidae) and the Halibut Hippoglossus stenolepis (Schmidt, 1904) (Pleuronectidae) E. M. Skorobrekhovaa, * and V. P. Nikishina, b aInstitute

of Biological Problems of the North, Far Eastern Branch, Russian Academy of Sciences, Magadan, 685000 Russia bNortheastern State University, Magadan, 685000 Russia *e-mail: [email protected] Received May 19, 2016

Abstract⎯We examined the structure of the tegument surface of the acanthocephalan Corynosoma strumosum and its surrounding capsule in paratenic hosts: the notched-fin eelpout Zoarces elongatus (Kner, 1868) and the Pacific halibut Hippoglossus stenolepis (Schmidt, 1904). In both cases, the capsules are “leucocytic” and have, in general, a similar structure but with a few peculiarities. Some of them are evidently caused by the different ages of capsules and others may be connected with the species of the host. The tegument surface of C. strumosum from eelpout is covered with a thick layer of glycocalyx, which is absent in acanthocephalans from halibut. The results suggest that the acanthocephalan C. strumosum is more adapted to the eelpout Z. elongatus and to the sculpin Myoxocephalus stelleri than to flatfish. Keywords: paratenic host, acanthocephalan, tegument, glycocalyx, capsule DOI: 10.1134/S1063074017010126

and paratenic hosts at the organism level in nature and experiment for more than 10 years. Our previous studies have shown that the kind of encapsulation varies depending on the species of host [8, 9, 11, 15]. In different hosts, three morphological forms of capsule around C. strumosum were identified that primarily differ in the ratio of fibroblasts and leucocytes. Thus, the acanthocephalan in the smelt Osmerus mordax dentex and the Pacific navaga Eleginus gracilis is surrounded with a capsule that mainly (or exceptionally) consists of fibroblasts [8]. The number of fibroblasts and leucocytes that form the capsule around the acanthocephalan in the white-spotted greenling Hexagrammos stelleri is approximately equal, whereas leucocytes are predominant in its composition in the sculpin Myoxocephalus stelleri and the yellow-finned sole Limanda aspera [11]. We hypothesized that these differences might be caused by a different degree of the balance of the interaction between an acanthocephalan and a host species [9, 11].

INTRODUCTION Paratenic parasitism, although found in various groups of animals, including many species of Acanthocephala, is a sparsely studied biological phenomena. Originally, it was considered to be a mechanism for accumulating and passing an invasion from an intermediate to a definitive host, which does not involve any advance in the development of parasite. However, in recent years this viewpoint has been recognized as being too simplified [12]. A deeper and adequate understanding of the essence of this phenomenon evidently requires the study of the interaction of the parasite and paratenic host. In particular, there is evidence that proves that acanthocephalans in such a host do not remain unchanged but continue to develop [14; et al.]. At the same time, merely fragmentary information on the structure and histogenesis of the cell capsule surrounding an acanthocephalan in a paratenic host existed until recently and sparse electron microscopic studies did not allow an unambiguous identification of the constituent cells of the capsule and description of the tegument structure of these parasites [9]. The authors of this paper have studied the interaction of the acanthocephalan Corynosoma strumosum

It has also been established that an acanthocephalan surrounded with a “fibroblastic” capsule produces a thick (up to 2 μm) layer of glycocalyx on its surface, whereas the layer of glycocalyx is absent in the acanthocephalan from the yellow-finned sole, which 49

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is enclosed in a “leucocytic” capsule [8, 15]. The degree of development of the glycocalyx could have been connected with the type of encapsulation of the acanthocephalan. However, further studies showed that specimens of C. strumosum parasitizing the sculpin are surrounded with “leucocytic” capsules similar to capsules found in the yellow-finned sole, but they form the layer of glycocalyx on their surface as in acanthocephalans that parasitize the smelt and navaga and are enclosed in “fibroblastic” capsules [11]. These results allowed us to suggest that the balance of interactions between an acanthocephalan and paratenic host species may be reflected not only in the kind of encapsulation, but also in the degree of development of glycocalyx. To verify this, we expanded the spectrum of paratenic hosts to include the notched-fin eelpout Zoarces elongatus and the Pacific halibut Hippoglossus stenolepis. These fish were selected because the halibut is systematically close to the yellow-finned sole that was studied previously and the notched-fin eelpout is close to the zoarcid Hadropareia middendorffii, in which, according to our preliminary data, acanthocephalans are also surrounded with “leucocytic” capsules. MATERIALS AND METHODS The material for the study was sampled from one specimen of notched-fin eelpout and one specimen of Pacific halibut. Sixty-three acanthocephalans were found in halibut 48.8 cm long (female): 2 were found inside the intestinal wall, 57 were on the intestine mesentery (Fig. 2a), and 4 on the liver. In the notched-fin eelpout 34 cm long (female), two acanthocephalans were found on the surface of the intestine mesentery. Encapsulated specimens were fixed with 2% glutaraldehyde in 0.1 M phosphate buffer, postfixed with 1% osmium tetroxide in 0.2 M phosphate buffer, dehydrated in a graded ethanol series, and embedded in Araldite-Epon. During dehydration, the specimens were contrasted with 1% uranyl acetate in 70% alcohol for 12 h. Semi-thin sections were cut on a LKB IV (Sweden) ultramicrotome, stained with a mixture of crystal violet and methylene blue (1 : 1), and examined in an Olympus CX 41 light microscope (Japan). Ultrathin sections were cut on a PT-PC ultramicrotome (Boeckeler Instruments, United States), contrasted with lead citrate, and examined in a JEM 1400 plus electron microscope (JEOL, Japan). RESULTS All investigated acanthocephalan specimens were enclosed in cell capsules (Figs. 1a, 2b, and 2c); the morphometric indices, organization, and cell composition of the capsules varied depending on the species of fish. The acanthocephalan body covering is a tegument organized as a typical symplast, the structure of its surface region also differed between the host species.

The Tegument Structure of the Acanthocephalan Corynosoma Strumosum and its Surrounding Capsule in the Eelpout Zoarces Elongatus Light microscope observations of the tegument structure of acanthocephalans revealed striated, vesicular, felt, and radial layers, as well as lacunae, nuclei, and a layer of homogeneous material on the outer tegument surface (Fig. 1b). Electron microscopy showed that this layer is the glycocalyx (Figs. 1c and 1d). The thickness of the glycocalyx varies from 0.5 to 2 μm; the outer boundary is sinuous, with deep concavities and, as a consequence, fragments of glycocalyx in sections often seem to be isolated from the main layer by cells of the surrounding capsule. In some areas, the glycocalyx layer is interrupted, while in others it is laminated with the result that light-colored and “hollow” spaces appear in it. A narrow (no more than 0.1 μm) layer of glycocalyx adjacent to the apical plasma membrane of the tegument has a higher electron density. Higher electron density of material is also observed where the glycocalyx is in contact with cells of the capsule, but in this case the thickness of the increased density layer reaches 0.4 μm. The glycocalyx is formed by densely organized filamentous material with the inclusion of two types of vesicles: small and larger. Small vesicles (up to 100 nm in diameter) are the most numerous and are found throughout the thickness of the glycocalyx (Fig. 1d), while larger vesicles (approximately 150 nm) are mainly concentrated at its outer boundary. The thickness of the striated layer including numerous invaginations of the outer plasma membrane does not exceed 0.6 μm (Fig. 1c). In the basal part of this layer, the invaginations are dilated in the form of cisterns to 0.4 μm in diameter; the cisternae make up the vesicular layer of tegument (Figs. 1c and 1e), which is clearly seen with a light microscope. Release of vesicles with a diameter that is more frequently 95–120 nm and less frequently reaches 160 nm and homogeneous contents of moderate electron density into the lumen of cisternae is often observed (Fig. 1f). Numerous mitochondria and lipid droplets are located at the base of the vesicular layer. In addition to the above layers, a tubular layer formed by invaginations of the inner plasma membrane is distinguished with an electron microscope in the basal part of the tegument. The capsule around the acanthocephalan is continuous, 131 to 206 μm thick (Fig. 1a). The base of capsule is composed of macrophages, eosinophils, neutrophils, and erythrocytes, which are present in an approximately equal number, as well as infrequent lymphocytes (Figs. 1b, 1c, 1g, and 1h); fibroblasts are lacking. Macrophages and granulocytes are relatively evenly distributed within the thickness of the capsule, lymphocytes are only found in its peripheral part. Erythrocytes in the upper portion of capsule are observed as large aggregations of up to 600 cells per section. They are also found within the thickness of the capsule and near the glycocalyx of an acantho-

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Fig. 1. The acanthocephalan Corynosoma strumosum from the notched-fin eelpout. (a) The general form of an encapsulated acanthocephalan; (b) fragment of the tegument of an acanthocephalan and the capsule around it; lacunae and nuclei are visible in tegument; (c) fragments of an acanthocephalan tegument with a glycocalyx on its surface and surrounding capsule at great magnification (oblique section); (d) small vesicles located within the glycocalyx layer; (e) fragment of the vesicular layer of the tegument, in which vesicles are located in cisternae; (f) fragment of Fig. 1e (framed) at great magnification, showing the formation of a vesicle as a result of secretion of material from the tegument cytoplasm into the cisterna; (g) eosinophil; (h) neutrophil. (a, b) Light microscopy; (c, d, e, f, g, h) electron microscopy. Designations: ac, acanthocephalan; cap, capsule; eo, eosinophil; er, erythrocyte; gl, glycocalyx; gr, granule; lc, lacuna; n, nuclei; ne, neutrophil; sl, striated layer of tegument; teg, tegument; v, vesicles; vl, vesicular layer of tegument. Scale (μm): (a) 100 ; (b) 10; (c) 2; (d and e) 1; (f) 0.5; (g and h) 2.


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Fig. 2. The acanthocephan Corynosoma strumosum from Pacific halibut. (a) Encapsulated acanthocephalans on the pyloric caecum mesentery of a fish (arrows); (b) acanthocephalan enclosed in a thin two-layered capsule, intensely stained with histological dyes; (c) acanthocephalan surrounded with a single-layered capsule, moderately stained; (d) fragments of tegument of intensely stained acanthocephalan and two-layered capsule around it; (e) fragments of tegument of moderately stained acanthocephalan and single-layered capsule around it; (f) fragment of tegument of intensely stained acanthocephalan with a thin layer of glycocalyx on its surface. (a, b, c, d, e) Light microscopy; (f) electron microscopy. Designations: ac, acanthocephalan; cap, capsule; gl, glycocalyx; ilc, inner layer of capsule; lc, lacuna; olc, outer layer of capsule; teg, tegument. Scale (μm): (b and c) 100; (d and e) 10; (f) 2.

cephalan in its “empty” spaces. Cells in the internal part of capsule are closely adjacent to each other, while in its external portion spaces between cells filled with electron-dense fibrous material occur. The part of cell that contacts the glycocalyx is completely destroyed. Some macrophages and neutrophils that remain intact produce wide outgrowths that pierce the surface region of the glycocalyx layer and sometimes reach to its middle. Macrophages appear as rounded cells containing an eccentric nucleus with few accumulations of heterochromatin and a distinct nucleolus. The cytoplasm includes a well-developed network of canals of the granular endoplasmic reticulum (GER), numerous mitochondria, light-colored vacuoles and large lipid droplets up to 5 μm in diameter. Electron-dense phagolysosomes comparable in size with the nuclei are rarely encountered in macrophages. Eosinophils of 7.8–11.6 × 6.7–9.8 μm are easily distinguished

through the light microscope due to the numerous dark-colored granules in their cytoplasm (Fig. 1b). The granules have a typical morphology: 1.0–1.4 μm in diameter, rounded or slightly elongate, with homogeneous electron-dense contents (Fig. 1g). The nuclei of eosinophils are eccentric, irregular in form, with small accumulations of heterochromatin, mainly near the nuclear membrane. Along with granules, the cytoplasm contains a well-developed Golgi complex and GER, as well as rounded or elongate mitochondria. Neutrophils were not readily identified by histological staining; nevertheless, they can be distinguished by their small size (5.7–10.4 × 4.1–7.2 μm), eccentric placement of a densely stained nucleus and a lightercolored cytoplasm. Via an electron microscope, their nuclei are characterized by irregular outlines and a moderate amount of heterochromatin that is predominantly found along the inner surface of the nuclear membrane (Fig. 1h). The granules of these cells differ


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from those of eosinophils in their smaller size, (0.6– 1.2 × 0.3–0.4 μm), elongated form, and nonhomogenous contents; an electron-dense component of the granules surrounds its electron-light central part as a rim. Neutrophils, like eosinophils, have a well-developed system of canals of the GER and Golgi zone. The Tegument Structure of the Acanthocephalan Corynosoma Strumosum and its Surrounding Capsule in the Halibut Hippoglossus Stenolepis Acanthocephalans collected from the halibut responded differently to histological staining. Most specimens were stained intensely (Figs. 2b and 2d) and in the dark thickness of their tegument we could only distinguish the fibers of the radial layer and the outlines of slightly lighter-colored lacunae and star-like nuclei with large dense nucleoli. In the tegument of less-intensely colored specimens, the fibers of the felt and radial layers, lacunae, and nuclei are clearly visible (Figs. 2c and 2e). Electron microscopic observations on all acanthocephalans revealed, apart from the above components of the tegument, the vesicular and tubular layers. Unlike acanthocephalans from the notched-fin eelpout, the vesicular layer of the tegument of an acanthocephalans from the Pacific halibut is weakly developed and consists of small vesicles, which include filamentous fibrillar structures. On the outer tegument surface of all acanthocephalans a narrow layer of glycocalyx (no more than 0.1 μm thick) that consists of a fine fibrillar material occurs (Fig. 2f). Light microscope observations showed that intensely stained specimens of acanthocephalans are enclosed in a relatively thin (33–101 μm) capsule of approximately the same thickness throughout its length that consists of two distinct layers (Figs. 2b and 2d). Less densely stained parasites were enclosed in a single-layered thicker (80–265 μm) capsule of varying thickness in different areas (Figs. 2c and 2e). The capsule structure in both cases differed also. The single-layered capsule is mainly formed by large rounded and closely spaced macrophages, as well as very few neutrophils and plasma cells. Few fibroblasts forming two-three rows of cells are found on the periphery of the capsule. The outer layer of the twolayered capsule is loose, light-colored and includes few capillaries; the inner layer is dark and more densely organized, with minimal intercellular spaces filled with collagen fibers and in some cases including lipid droplets (Fig. 2d). The basic cell components of two-layered capsule are macrophages and fibroblasts, as well as an insignificant number of neutrophils and plasma cells. The macrophages of the inner capsule layer are large (8.1–14.5 × 7.9–11.6 μm), oval and include a rounded eccentric nucleus with a distinct nucleolus and a few electron-dense phagolysosomes and lipid droplets (Fig. 3a). Fibroblasts differ from macrophages in their flattened form, elongated nucleus, and long processes (Fig. 3b). Their cytoplasm RUSSIAN JOURNAL OF MARINE BIOLOGY

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contains canals of the GER, rounded mitochondria, and multiple small vesicles concentrated along the inner surface of the plasma membrane. The neighboring fibroblasts are connected to each other by typical desmosomes (Fig. 3b). Unlike the inner layer of the capsule, the intercellular spaces in its outer layer are larger and visually contain a much greater amount of collagen fibers, which make up a loose network. In addition to fibroblasts, fibrocytes distinguished by a characteristic high nucleus-plasma ratio and minimal number of organelles occur. Cells of both forms are generally arranged in regular rows around an acanthocephalan (Fig. 3c). Macrophages in the outer capsule layer are represented by two types. Macrophages of the first type were relatively evenly scattered over the entire layer and similar in their morphological features to macrophages of the inner layer (Fig. 3a). Macrophages of the second type make up large aggregations (Fig. 3d). These cells are peculiar in having multiple phagolysosomes that occupy the greater part of their cytoplasm and often exceed the nuclei in size while lacking the lipid droplets found in macrophages of the inner capsule layer. The contents of phagolysosomes are electron-dense, heterogeneous, sometimes with structures that resemble bundles of densely organized fibers. Neutrophils are localized singly in the inner capsule layer and as small aggregations in the outer layer. They are characterized by rounded or oval nuclei with an electron-light karyoplasm and a small amount of heterochromatin (Fig. 3e). A peculiarity of these cells is the presence of elongated granules (0.6–1.0 × 0.2–0.3 μm) with fibrillar contents. Along with granules, short canals of the GER and rounded mitochondria are observed in the cytoplasm. Plasma cells are distinguished by multiple cisternae of the GER filling almost the entire cytoplasm and widened (to 170 nm) perinuclear spaces (Fig. 3f). The cells are relatively small, rounded or elongate-oval, with the nuclei shifted to the cell periphery. In addition to the GER cisternae, the cytoplasm contains few relatively large mitochondria and one–two Golgi zones. DISCUSSION The results of this study show that the acanthocephalan Corynosoma strumosum in the notched-fin eelpout and the Pacific halibut is surrounded with a “leucocytic” capsule that is primarily formed by leucocytes and is externally similar in structure to the capsule of the acanthocephalans from the yellowfinned sole or Steller’s sculpin [11, 15]. At the same time, despite the fundamental similarity of their organization, the investigated capsules of an acanthocephalans from both species of fish somewhat differ in the composition and the quantitative ratio of the constituent cell components. Thus, the capsule of the acanthocephalans from Pacific halibut includes, along with leucocytes, a variously developed pool of fibroNo. 1

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Fig. 3. The cell composition of the capsule surrounding the acanthocephalan Corynosoma strumosum in Pacific halibut (electron microscopy). (a) Macrophage; (b) fibroblasts from inner capsule layer; (c) fibrocytes from outer capsule layer, wide intercellular spaces are filled with loose collagen fibers; (d) aggregation of macrophages containing numerous variously-sized phagolysosomes in the outer capsule layer; (e) neutrophil; (f) plasmocyte. Designations: cf, collagen fibers; d, desmosomes; fb, fibroblasts; fc, fibrocytes; ger, granular endoplasmic reticulum; gr, granules; l, lipid droplets; ma, macrophages; n, nuclei; pf, processes of fibrocytes; ph, phagolysosomes. Scale (μm): (a and b) 2; (c and d) 5; (e and f) 2.

blasts and synthesized collagen fibers, while the capsule of the acanthocephalans from the notched-fin eelpout is mainly formed by leucocytes and a relatively small number (in percentage ratio) of erythrocytes; no fibroblasts were found.

According to the existing views, the presence of leucocytes in the composition of capsule is indicative of an inflammatory response of the host to invasion [1]. It is also known that the inflammatory process consists of alteration, exudation, and proliferation


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stages; apart from this, it includes leucocytic migration to the source of inflammation at initial stages and fibroblast migration at the concluding stage [1]. In this regard, the absence of fibroblasts in the capsule from the notched-fin eelpout seems, to some extent, paradoxical. However, there is no basis to consider this fact as a peculiarity connected with the species of the host. Taking the above remark about the order of cell migration to an inflammation source into account, it can be supposed that the lack of the fibroblast component in the capsules may be due to their young age when mass migration of fibroblasts to the parasite has not yet begun. Possibly for the same reason, capsules from the notched-fin eelpout include large accumulations of erythrocytes that evidently entered the body from the wound inflicted by the acanthocephalan when penetrating the intestinal wall of the fish. Moreover, certain differences in the composition of leucocytes that form capsules (in capsules from Pacific halibut, macrophages prevailed among leucocytes; in capsules from the notched-fin eelpout eosinophils and neutrophils were present along with macrophages) may be caused by the different ages of capsules, as well as the species of host. We note that in another eelpout Hadropareia middendorffii (which is systematically close to notched-fin eelpout) capsules around acanthocephalans are also “leucocytic” but three-layered and fibroblasts are the necessary components of the middle and especially the outer layer of the capsules (our unpublished data). This location of fibroblasts indicates their later migration to the parasite, when the layer of leucocytes has surrounded it. The pattern of location of the fibroblasts described in capsules from the Pacific halibut was similar to that observed in capsules from the yellow-finned sole and Steller’s sculpin [11, 15]. Finally, unlike other capsules, one of the previously investigated capsules from the Steller’s sculpin had in its composition only sparse collagen fibers, which may be connected with its young age [11]. Thus, the above data allow us to consider the absence of the fibroblast component in the investigated capsules from the notched-fin eelpout as being temporary and caused by the initial stage of capsule formation. The next stage is intensive migration of fibroblasts to the parasite, their inclusion in the composition of the capsule, more exactly in its outer region, and the formation of collagen fibers by fibroblasts. This scheme is indirectly supported by the differences in the structure of capsules from the Pacific halibut. The single-layered capsules around some acanthocephalans in this host, which consist of a large number of macrophages and relatively few fibroblasts, represent a younger form of invasion. The two-layered organization of capsule and the presence of a much greater quantity of fibroblasts are indicative of a longer migration of these cells to the capsule, resulting in closer packing of earlier migrating leucocytes and formation of the inner capsule layer by leucocytes. Moreover, the darker coloration of acanthocephalans RUSSIAN JOURNAL OF MARINE BIOLOGY

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enclosed in two-layered capsules may suggest some changes in the parasite during its continual presence in its paratenic host. A similar scheme has been observed in the lizard Lacerta agilis infected with corynosomes in experiments [16]. However, the lizard is not a natural paratenic host of this acanthocephalan; therefore, direct experimental investigations of the formation of the capsule around acanthocephalan in a natural paratenic host are needed for an unambiguous verification of the scheme. The differences in the morphology of the acanthocephalan C. strumosum, which parasitizes the Pacific halibut and the notched-fin eelpout, are found not only in the capsule structure but also in the structure of the parasite covering, specifically the degree of development of the glycocalyx on the tegument surface. In acanthocephalans from the halibut, as well as from the sole [11], a very thin (no more than 0.1 μm) layer of glycocalyx was found. Moreover, in parasites from these fish the vesicular layer of the tegument is weakly defined. In contrast, acanthocephalans from the notched-fin eelpout are characterized by a thick glycocalyx layer and widened elements of the vesicular layer. Similar features were described in acanthocephalans from Steller’s sculpin [11], as well as in cystacanths of Polymorphus magnus and P. strumosoides from intermediate hosts [3, 4, 7]. The secretion of material in the form of vesicles from the tegument into the lumen of cisternae of the vesicular layer in notched-fin eelpout resembles the phenomenon that was described previously in the vesicular layer of cystacanths of P. magnus and was considered as an element of the mechanism of formation of glycocalyx [4, 7]. However, in the case of Polymorphus, such a secretion was not frequently observed and the glycocalyx layer was homogeneous and did not include vesicles found in the glycocalyx of acanthocephalans from the notched-fin eelpout. This difference can be accounted for by the different duration of the persistence of the parasites in the host and, consequently, the different periods of glycocalyx formation. Thus, in acanthocephalans from the eelpout this process was not yet completed, while the cystacanths of Polymorphus, as well as the glycocalyx layer on their surface, were quite formed. A similar process of secretion of vesicular material from cytons of the cyst wall tegument onto the cyst surface has been described in the cysticercoids of some hymenolepidid cestodes that have a cyst covered with a similar thick layer of glycocalyx [2, 5]. Hence, it can be supposed that the widening of the terminal portions of “canals” of the striated layer (cisternae of vesicular layer), as well as the release there of small vesicles from the tegument cytoplasm followed by their secretion onto the surface of the parasite, are the stages of the formation of the massive layer of glycocalyx. The results of the present study expand our understanding of the variety of interactions between acanNo. 1

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thocephalans and paratenic hosts. Morphologically, this variety is manifested in the peculiarities of the structures of capsules that surround parasites and in the organization of the acanthocephalan tegument, primarily the glycocalyx on its surface. We previously suggested that by analogy with cestodes [10], the capsule structure and the degree of development of glycocalyx correspond to the degree of adaptation of an acanthocephalan to a particular species of host [9]. Our results show that even with the same form of the interactions that involve the formation of “leucocytic” capsule, there are certain morphological peculiarities that are apparently caused by the species of paratenic host. These peculiarities are vividly demonstrated by the facts of the formation or nonformation of a thick glycocalyx on the tegument surface of acanthocephalans that parasitize paratenic hosts (tissue parasitism in the broad sense of the word) that were observed in flat worms [5]. Thus, the differences in the structure of capsules around the acanthocephalan C. strumosum the parasitizes the notched-fin eelpout and the Pacific halibut may be due both to the age of the capsules (the quantitative ratio of fibroblasts and leucocytes) and to the species of host (leucocytic composition). The presence or absence of a thick layer of glycocalyx on the tegument surface of corynosomes probably also depends on the species of host. However, these conclusions should be confirmed by further investigations of acanthocephalans from more species of hosts. Nevertheless, comparing the present results with previously published data and taking the likely protective function (among others) of the helminth’s glycocalyx into account [5, 6, 13], it can be suggested that the acanthocephalan C. strumosum is more adapted to the notched-fin eelpout and Steller’s sculpin than to the flatfish, although it is also surrounded with a “leucocytic” capsule in the latter fishes. ACKNOWLEDGMENTS This study was supported by the Russian Foundation for Basic Research, project no. 15-04-01418 and the Presidium of the Far Eastern Branch of the Russian Academy of Sciences, project no. 15-1-6-015o. REFERENCES 1. Bykov, V.L., Tsitologiya i obshchaya gistologiya (funktsional’naya morfologiya kletok i tkanei cheloveka) (Cytology and General Histology (Functional Morphology of Cells and Tissues of Humans), St. Petersburg: SOTIS, 2007. 2. Krasnoshchekov, G.P. and Nikishin, V.P., Ultrastructure of the protective envelopes of the larvae of cestodes, in Ekologiya i morfologiya gel’mintov pozvonochnykh Chukotki (Ecology and Morphology of Helminths of Vertebrates in Chukotka), Moscow: Nauka, 1979, pp. 116–132.

3. Nikishin, V.P., The fine structure of the metasome wall of a cystacanth of the acanthocephalan Polymorphus strumosoides (Acanthocephala, Polymorphidae), Parazitologiya, 1986, vol. 20, no. 5, pp. 403–408. 4. Nikishin, V.P., Tsitomorfologiya skrebnei (pokrovy, zashchitnye obolochki, embrional’nye lichinki) (Cytomorphology of Acanthocephalans (Coverings, Protective Membranes, Embryonic Larvae)), Moscow: GEOS, 2004. 5. Nikishin, V.P., Morphofunctional variety of the glycocalyx in tapeworms, Usp. Sovrem. Biol., 2016, vol. 136, no. 5, pp. 523–543. 6. Nikishin, V.P. and Lebedev, D.V., Experimental evidence of the defense role of the exocyst in the metacestode Microsomacanthus lari Belogurov et Kulikov, in Spasskaja, 1966 (Cestoda: Hymenolepididae), Russ. J. Mar. Biol., 2011, vol. 37, no. 1, pp. 80–83. 7. Nikishin, V.P., Pluzhnikov, L.T., and Leonov, S.A., The ultrastructure of covers in cystacanths of Polymorphus magnus (Acanthocephala, Polymorphidae), Parazitologiya, 1994, vol. 28, no. 1, pp. 52–59. 8. Nikishin, V.P. and Skorobrekhova, E.M., Encapsulation of an acanthocephalans Corynosoma sp. in two reservoir host species, Dokl. Biol. Sci., 2007, vol. 417, pp. 462–464. 9. Nikishin, V.P. and Skorobrekhova, E.M., Host–parasite interactions in Acanthocephala (morphological aspect), Usp. Sovrem. Biol., 2015, vol. 135, no. 2, pp. 203–221. 10. Pronina, S.V. and Pronin, N.M., Vzaimootnosheniya v sistemakh gel’minty–ryby (Interrelationships in Helminth–Fish Systems), Moscow: Nauka, 1988. 11. Skorobrekhova, E.M. and Nikishin, V.P. Dependence of the structure of the capsule surrounding the acanthocephalan Corynosoma strumosum on the species of its natural paratenic host, Biol. Bull., 2014, vol. 41, no. 4, pp. 333–348. 12. Sharpilo, V.P. and Salamatin, R.V., Paratenicheskii parazitizm: stanovlenie i razvitie kontseptsii. Istoricheskii ocherk, bibliografiya (Paratenic Parasitism: Origins and Development of the Concept: Historical Assay, Bibliography), Kiev: LOGOS, 2005. 13. Lumsden, R.D., Surface ultrastructure and cytochemistry of parasitic helminths, Exp. Parasitol., 1975, vol. 37, no. 2, pp. 267–339. 14. Marchand, B. and Grita-Timoulali, Z., Comparative ultrastructural study of the cuticle of larvae and adults of Centrorhynchus milvus Ward, 1956 (Acanthocephala, Centrorhynchidae), J. Parasitol., 1992, vol. 78, no. 2, pp. 355–359. 15. Skorobrekhova, E.M. and Nikishin, V.P., Structure of capsule surrounding acanthocephalans Corynosoma strumosum in paratenic hosts of three species, Parasitol. Res., 2011, vol. 108, no. 2, pp. 467–475. 16. Skorobrekhova, E.M., Nikishin, V.P., and Lisitsyna, O.I., Structure of capsule around acanthocephalan Corynosoma strumosum from uncommon paratenic hosts – Lizards of two species, Parasitol. Res., 2012, vol. 110, no. 1, pp. 459–467.


Translated by T. Koznova Vol. 43

No. 1

2017