Caryophyllaeus fimbriceps Annenkova-Chlopina, 3919 and Khawia sinensis Hsü, 1935: Occurrence in Hungary and Morphology

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1 Caryophyllaeus fimbriceps Annenkova-Chlopina, 3919 and Khawia sinensis Hsü, 1935: Occurrence in Hungary and Morphology Dr. Éva MURAI Dr. Kálmán MOLNÁR Zoological Department of the Hungarian Natural History Museum, Budapest Veterinary Medical Research Institute of the Hungarian Academy of Sciences, Budapest "Caryophyllaeus fimbriceps Annenkova-Chlopina, 1919 and Khawia sinensis Hsü, 1935: Occurrence in Hungary and morphology" - Murai, E. - Molnár, K, - Parasit. Hung ABSTRACT. On the ground of zoogeographical considerations the authors put forward the wiev that K. sinensis of the carp was introduced to Hungary from the Trans-Carpathian area by natural route through the river Tisza. Morphological studies of the carp parasites C. fimbriceps and K. sinensis by histological methods resulted in certain modifications of the original descriptions of K.sinensis. Six species of the family Caryophyllaeidae (Caryophyllaeus brachycollis Janiszewska, 1951, C. fimbriceps Annenkova-Chlopina, 1919, C.laticeps /Pallas, 1787/, Paracaryophyllaeus dubininae Kulakovskaya, 1961, Biacetabulum appendiculatum (Szidat, 1937/, Ca~ryophyllaeides fennica /Schneider, 1902/) were formerly known to occur in Hungary (EDELENYI, 1967; ERGENS et al., 1974; MOLNÁR, 1970; MATSKÁSI et al., 1-971). The occurrence of a seventh species, Khawia sinensis Hsü, 1935, has recently been reported by MOLNÁR and BUZA (1975). According to Russian authors (KULAKOVSKAYA and KRO- TAS, 1961; IVASIK et al., 1968), among the Caryophyllaeidae species found in Europe, two have been of economic importance, K. sinensis and C. fimbriceps. The latter has been erroneously regarded as synonymus with C. laticeps by several authors. KULA KOVSKAYA and KROTAS hold the view that K. sinensis, which had been introduced with amur carps imported from the Far East, is gradually superseding C. fimbriceps, which had formerly been very widely spread in Europe. The presence of K. sinensis in the European territory of the Soviet Union was reported first by KULAKOVSKAYA and KRO TAS (1961) and its spread beyond the Carpathian mountains by IVASIK et al. (1970). PRIBYSLAVSKY et al. (1965) in Czechoslovakia found a Khawia specimen, which they regarded as K. sinensis but on the basis of epizootological considerations characterized it as an indigenous parasite for Europe. The anatomy of various Caryophyllaeidae species has been extensively studied. WILL (1893) dealt in great detail with C. laticeps (C. mutabilis), CALETINE and ULMER (1961) with K. iowensis and MACKIEWITZ (1972) elaborated a parasitological rewiew of the entire group. However, the anatomical details of the two species parasitic in carps in Hungary (C. fimbriceps. K. sinensis) were only known from the original descriptions (AN NENKOVA-CHLOPINA, 1919; HSÜ, 1935) and from later studies of KULAKOVSKAYA and KROTAS (1961). The present studies were carried out to obtain more information on the morphological details of these two species of economically important carp parasites and to assess the frequency of occurrence of K. sinensis in the home carp populations.

2 Material and Methods After the first demonstration of K. sinensis in this country in the autumn of 1974, post mortem examination of 500 three summer carps taken from pond farms located in the catchment areas of the rivers Danube and Tisza was carried out to estimate the incidence of the parasite in Hungary. The C. fimbriceps exemplars used in the present study were preserved specimens collected earlier. The tapeworms found in the gut of the carps studied were fixed in hot formaline 5%. Some worms were used for in toto preparations, which were stained with BLACHIM carmine, HCl-carmine and haemalaun; those used for histological examination were embedded in paraffine, cut into sections in the longitudinal, sagittal and transversal planes, and were stained with haematoxylin and eosin. x Results The incidence of K. sinensis infection was found to be 35% in 300 carps taken from the ponds associated with the river Tisza, whereas among the 200 carps originating from ponds in the Danube watershed area only a single fish harboured a single Khawia parasite, A single C. fimbriceps was found in the entire group studied, although in our earlier collections this parasite had been regularly encountered in carp hosts taken of natural habitats, above all of the river Danube and Lake Balaton. Description of Caryophyllaeus fimbriceps Annenkova-Chlopina, 1919, on the basis of exemplars found in Hungary Host: Cyprinus carpio - Localization: anterior third of the gut - Intensity of infection: 1-30 parasites - Locality: river Danube. Small Caryophyllaeinae species (Fig. 1 ), measuring mm in length and up mm in width. The scolex is slightly frilled, 1,5-1,8 by 1,2 mm in dimension. A somewhat tapering neck is present behind the scolex. The first vitellaria are 1 mm away from the scolex followed anteriorly to the first testes. Both structures localize in the medullary parenchyma (Fig. 3). The anterior four fifths of the body are filled by the vitellaria and testes which are also extending along the cirrus pouch (Fig. 4). The latter, as well as the ovary, uterus, Mehlis' gland and the postovarian vitellaria all localize in the posterior 2-3 mm long portion of the body. The excretory cariais pass in the cortical parenchyma and unite at the posterior pole of the body to from the terminal excretory bladder and excretory duct. The bladder is 150 u in diameter, the terminal excretory duct is 100 u long and p. wide. Reproductive system. The testes are roundish bodies, p in diameter. They localize in the medullary parenchyma and are surrounded on each side by vitellaria. The first testes are 1,5 mm away from the scolex, the last ones are found in level with the anterior half of the cirrus pouch (Fig. 4). The cirrus pouch is very large related to the body, measuring x p, and is surrounded by a muscular wall. The male genital pore opens into the íienítal atrium in front of the uterovaginal pore. The cirrus fills the entire space within the cirrus pouch while at rest, but extends a 400,u long by u wide portion beyond the genital atrium at erection (Fig. 5). The vas deferens forms several convolutions before reaching the cirrus pouch and can further be followed Thanks are due to dr. L. BUZA and Mr. F. SZIKLAI (Central Veterinary Institute, Budapest), who kindly supplied part of the test materials, and to Mrs. Emese S. FARKAS, Mrs. Etelka P. VAJDA and Mr. M. MÁRTONKA, for the post mortem examinations and processing of the histological preparations.

3 Figs. 1-2: 1: Caryophyllaeus fimbriceps (A: anterior extremity; B: posterior half of the body), 2: Khawia sinensis (A: anterior extremity; B: posterior third of the body) (Figs orig.)

4 up in the median line of the body over a distance of 1-2 mm. The bulk of the vas deferens, a pyramidal structure x p in size, pushes the testes and vitellaria to one side (Fig. 3). The vagina and uterus fuse above the isthmus of ovary to form an utero-vaginal canal, which opens into the genital atrium beneath the cirrus (Fig. 6), The wall of the uterus is covered by well-developed uterine glands. The lumen of the uterus p wide. The convolutions of the uterus extend up to the cirrus anteriorly and pass beyond the isthmus of the ovary posteriorly. The uterine coils number 9 to 11. The vagina localizes in the median line of the body and the cells surrounding its wall show a marked affinity to stain. Anterior to the isthmus of the ovary the vagina widens to form the seminal receptacle, which measures p by p (Fig. 7). The ovary is a H- shaped, compact structure (Figs. 7 and 8); its lateral lobes are 1, 1 to 1, 5 mm long. The isthmus of the ovary is u wide, extending over the entire width of the medullary parenchyma. The posterior part of the lobes is narrower and longer than the anterior part. The bulky Mehlis gland, p. in diameter, localizes behind the isthmus of the ovary (Fig. 8). The seminal receptacle fuses with ootyp and vitelloduct dorsally from the isthmus in the Mehlis gland area, where the uterus begins. The vitellaria, p in diameter, localize along with the testes in the medullary parenchyma in the anterior four fifths of the body. Vitellaria and testes are variably present along the anterior half of the cirrus pouch (5-6 testes at both sides), but only vitellaria, in number, can be found in the lateral field between cirrus pouch and ovary. The few postovarian vitellaria consist of about 50 vitelline follicles. The eggs are large, by p in size. Description of Khawia sinensis Hsü, 1935, on the basis of the present findings riost: Cyprinus carpio - Localization: anterior third of the gut - Locality: Pond farms in the catchment area of the river Tisza. Large Lytocestinae species (Fig. 2), measuring mm in length and up to 2 mm in width. The anterior margin of the scolex is conspicuously frilled and measures 2,0-2,5 by 1,2-1,5 mm. A 3-4 mm long, slightly tapering "neck region" is present between scolex and the first vitellaria. The first testes are found 1,0-1,5 mm away from the latter. The vitellaria localize in the cortical parenchyma, the testes in the medullary parenchyma (Fig. 9). Vitellaria and testes are numerous filling the anterior five sixth of the body. Testes extend to the cirrus pouch. Along the sides of this structure neither testes nor vitellaria are found (Fig. 11). 3 to 5 vitellaria localize between cirrus and ovary. The postovarian groups of vitellaria are found in both cortical and medullary parenchyma (Fig. 17). The excretory canals are irregularly arranged in the cortical parenchyma, and fuse to form a terminal vesicle, u in diameter, at the posterior end of the body. The vesicle is continuous with a terminal excretory duct, 160 u long and 40 p wide (Fig. 18). Figs. 3-8: Transversal sections of Caryophyllaeus fimbriceps (3: section at the level anteriorly to cirrus pouch; 4: section at the level of the centre of cirrus pouch; 5: section at the level of the cirrus; 6: section of the atrium genitale accepting the uterovaginal canal; 7: section at the level of the isthmus of ovary; 8: section of Mehlis'gland). Abbreviations: c = cirrus; c. p. = cirrus pouch; ex - terminal excretory duct; g a = genital atrium; Mg. = Mehlis'gland; m. 1. = long musculature; ov. = ovary; r s = receptaculum seminis; t = testes; u. = uterus; u. p. = uterovaginal pore; ut.-v. ='uterovaginal canal; vag. = vagina; v. d. = vas deferens; vit. = vitellaria.

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7 Reproductive system. The first testes are found 3-4 mm behind the scolex, the last ones at the anterior pole of the cirrus pouch. The anterior testes are smaller ( p in diameter) than the posterior ones ( p in diameter) (Fig. 9-10). The cirrus pouch is ovoid, and x p in size. The cirrus is "folded" in the posterior two thirds of the pouch in the inactive state, but forms a 640 u long structure with muscular walls at erection (Fig. 11), The convoluted vas deferens localizes in the anterior third of the cirrus pouch and is also seen anteriorly outside it; the extra-saccular portion is 1,0-1,5 mm long and 0,5-0^ mm wide, and neither vitellaria nor testes are seen in the pyramid-shaped area filled by it. The male genital pore opens into the genital atrium anterior to the utero-vaginal portion (Fig. 11). At 240 ja distance from the spot of the utero-vaginal fusion the muscular utero-vaginal canal takes a funnel shape by widening up to p in diameter and then joins to the genital atrium (Fig. 12). Neither the utero-vaginal canal, nor the cirrus is bearing cuticular spines.' The uterus forms convolutions between cirrus pouch and ovarian isthmus, and 3-4 convolutions posterior to the isthmus. The lumen of the uterus is p in diameter, its wall is surrounded with very well developed uterine glands (Fig. 13). The vagina is 5-6 mm long, 40 p in diameter, surrounded by a very thin layer of glandular cells stain deeper (Fig. 13). The vagina takes a slightly undulating course in the median line of the body towards the isthmus of the ovary, and distends to form a seminal receptacle in level with the isthmus. The seminal receptacle x p in size, localizes behind the ovarian isthmus and bends obliquely over the right lobe of the ovary (Figs. 14 and 15). The ovary is H-shaped, 3-4 mm long and fills the entire space within the medullary parenchyma. The intrinsic structure of the ovary is characteristically reticular (Figs ). The posterior part of the ovarian lobes is longer, whereas the anterior part is thicker, compared to one another. The isthmus is p in diameter. Many vitellaria surround the poles of the posterior lobes. The bulky Mehlis gland, 0,8-1,0 mm in diameter, fills the entire space between posterior ovarian lobes and postovarian vitellaria (Fig. 16), The ootyp localizes in the posterior part of the ovarian isthmus, behind the seminal receptacle. The vitelloduct and oviduct both open into the ootyp and at this spot commences the - uterus. Vitellaria localizing in the anterior third of the body are a,those localizing anterior to the cirrus pouch are p in diameter. There are about 500 postovarian vitelline follicles, ,u in diameter each. The eggs are small, by u in size. Discussion The present findings clearly indicate that the carp parasite K. sinensis has fairly widely spread in the pond farms located in North-Eastern Hungary and generally in the catchment area of the river Tisza, whereas its spread to the Danube watershed area is now in the initial phase. If the geographical localization of the distribution area is taken into consideration, it is clear that the parasite entered the country from the Trans-Carpathian area of the Soviet Union via the river Tisza. Since no carps were imported to Hungary in the recent past, introduction of K. sinensis with imported hosts can be excluded. In Poland (PANCZIK and ZELAZNY, 1974) and the German Democratic Republic Figs. 9-18: Transversal sections of Khawia sinensis (9: section at the level of the first third of the body; 10: section at the level anteriorly to the cirrus pouch; 11: section at the level of atrium genitale; 12: enter of the uterovaginal canal into the genital atrium; 13: position of the uterus convolutions and the vagina posteriorly to the cirrus pouch; 14: section at the level of the isthmus of ovary; 15: receptaculum seminis under the isthmus of ovary; 16: section of the Mehlis'gland; 17: group of postovarian vitellaria; 18: terminal excretory duct, Photo MOLNÁR, K. )

8 (MATTHEIS and SP AN GENBERG, 1974), however, this parasite has likely been introduced by imported fishes. The demonstration of a single Khawia. identified as K. sinensis in a carp in Czechoslovakia in 1963 (PRIBYSLAVSKY et al., 1965) was a confusing event; the authors finally considered that species as indigenous in the Danube basin, because they excluded the possibility of the introduction. Since, however, no further occurrence of the species had been reported in Czechoslovakia during the last 10 years and the parasite was found to differ from K. sinensis in certain morphological details, the specimen, described by PRIBYSLAVSKY et al. may weu have represented another species. No conclusions have been drawn in respect of the frequency of occurrence of C. fimbriceps, because the period in which the present study was conducted did not coincide with the peak occurrence of the species, which is during spring and summer. The morphological characters observed in this study correspond with those described by KULAKOVSKAYA and KROTAS (1961) for both K. sinensis and C. fimbriceps, but certain important details of the former do not accord with HSU's (1935) original description. Our exemplars showed different proportions in the dimensions of testes and viteuaria than those given by HSÜ, the testes of our specimens being larger. Against this, CALETINE and ULMER (1961) mention the larger size of viteuaria in relation to testes as an important differentiating feature from other species. According to HSÜ, the uterovaginal duct bears spines au over its inner surface, but we failed to find these structures in the exemplars studied. We found that the uterovaginal duct forms a funnel-like distension, «in diameter, beneath the cirrus pouch, but HSÜ made no mention of this important morphological detail. Convolutions of the vas deferens anterior to the cirrus pouch were found by HSÜ over an 50 u long area, whereas in our specimens the pyramid-shaped area occupied by convolutions of the vas deferens was least 1 mm long. Summary The incidence of the carp parasite K. sinensis was found to be 35 % in the pond farms associated with the catchment area of the river Tisza, whereas only sporadic incidence was noted in carp ponds localizing in the Danube watershed area. The conclusion lies close at hand that the parasite spread to Hungary from the Soviet Union, where it was indigenous, through the river Tisza. The Khawia species recently found in Hungary is clearly identical with the one fairly common and indigenous in the Soviet Union, originated from the Far East. However, the important morphological deviations between our specimens and the parasite originally described by HSÜ (1935) as K. sinensis may rise the suspicion of non-identily of these two parasites. Nevertheless, we belive that the species found by us is identical with HSU's parasite and the aforementioned differences are due to errors in the original description, because even in HSÜ's original drawings the testes are obviously larger than the vitellaria. The morphology 1 of K. sinensis and another economically important caryophyllaeida, C. fimbriceps, was studied by histological methods. C. fimbriceps corresponded in every respect with the related literary data, but certain important details of K. sinensis differed from those given in the original description. These deviations were ascribed to inadequacies of the original description. It is pointed out that - contrary to what is said in the original description - testes of K. sinensis are in fact larger that the vitellaria. sa

9 MURÁI, É. MOLNÁR, K.: Vizsgálatok a Caryophyllaeus fimbriceps Annenkova-Chlopina, 1919 és a Khawia sinensis Hsü, 1935 fajok magyarországi elterjedéséről és morfológiájáról Magyarországon a pontyok K. sinensis iertőzöttsége a Tisza vízgyűjtő területén levő gazdaságokban eléri a 35 %-ot, ezzel szemben a Duna vízgyűjtő területén e faj csak sporadikusan fordul elő. A szerzők véleménye szerint a K. sinensis természetes úton, a Tisza közvetítésével a Szovjetunióból terjedt át Magyarországra. A szerzők szövettani módszerekkel tanulmányozták a magyarországi pontyokban élő két faj, a C. fimbriceps és a K. sinensis morfológiáját. A C. fimbriceps vonatkozásában a szakirodalmi adatoknak megfelelő eredményt kaptak. A tanulmányozott K. sinensis példányok több tekintetben is eltérnek az eredeti leírástól, az eltéréseket azonban a szerzők az eredeti leírás hiányosságának tulajdonítják. Korrekcióra szorul a herék és a szikmirigyek nagyságának aránya, A herék - akárcsak egyéb Khawia fajokban - nagyobbak a szikmirigyeknél, ami az eredeti rajzokon is látható és ellentétben áll az eredeti leirással. References ANNENKOVA-CHLOPINA, N, P. (1919): Dva novikh vida paraziticheskikh chervey roda Caryophyllaeus, naydennikh v kishechnike karpovikh rib. - Izv. Ross. Akad. Nauk., CALE TINE, R. L. - ULMER, M.J. (1961): Khawia iowensis n, sp. (Cestoda: Caryophyllaeidae) from Cyprinus carpio L. im Iowa. - J.Parasit,, EDELÉNYI, B. (1969): A Tisza halaiban élősködő férgek és dinamikus jelentkezésük. - Debreceni Agrártudományi Főiskola Tudományos Közleményei, , ERGENS, R, - GUSSEV, V, A. - IZYUMOVA, N. A. - MOLNÁR, K. (1964): Parasite fauna of fishes of the Tisa river basin. - Rozpravy Ceskoslovenské A. V. Roda Matematickych a Prírodních Ved., 85. 2, HSÜ, H.F. (1935): Contribution a l'étude des Cestodes de Chine. - Rev. Suisse Zool., IVASIK, V.M. - FEDUSCHAK, N.J. -MASLENNIKOVA, K.I. (1970): Über die parasitologische Situation in den Teichwirtschaften des Karpaten-Rayons. - Z. Fischerei N. F IVASIK, V.M. - KARPENKO, I. - KULAKOVSKAYA, O.P. - FEDUSCHAK, N.J. (1968): Nyugat-ukrajnai tógazdaságokban észlelt hahvadék megbetegedések. - Magy. Állatorvosok Lapja, KULAKOVSKAYA, O.P. - KROTAS, P.A. (1961): O Khawia sinensis Hsü (Caryophyllaeidae, Cestoda) - parasite, zavezennom s Dalynevo Vostoka v karpovie khozyaystva zapadnikh oblastey SSSR. - Dokladi AN SSSR., MACKIEWITZ, J. S. (1972): Caryophyllidea. (Cestoidea): A review. - Exp. Parasit., MATSKÁSI, I. - MÉSZÁROS, F. - MURAI, É. (1971): A balatoni halak helminthológiaj vizsgálatának eredményei. - ÁUattani Közlemények, , MATTHEIS, T, H. - SPANGENBERG, R. (1974): Khawia sinensis als Parasit des Karpfens (Cyprinus carpio) in der DDR. - Z. Binnenfisch. DDR, 21_ MOLNÁR, K. (1970): Beiträge zur Kenntnis des Fischparasiten-fauna Ungarns, VI, Cestoda, Nematoda, Acanthocephala, Hirudinea, - Parasit, Hung.,

10 galandfér- MOLNÁR, K. - BUZA, L. (1975): Pontyok Khawia sinensis Hsü, 1935 okozta gessége Magyarországon. - Halászat (in press). PANCZYK, J. - ZELAZNY, J. (1974): Khawioza i bothriocefaloza karpi - nowe choroby pasozytnicze stwierdzone w Polsce. - Gosp, rybna, PRIBYSLAVKY, J. - JILEK, J, - LUCZKY, Z. (1965): Die Helminthen der Fische des Stausees Kninicka, neu für die Fauna CSSR. - Vestn, Ceskosklov. Spol. Zool., WILL, H. (1893): Anatomie von Caryophyllaeus mutabilis Rud, Ein Beitrag der Cestoden. - Z. Wiss. Zool., , Received: 10 May, 1975 Dr. MURAI, É. Zoological Department of the Hungarian Natural History Museum 1088 Budapest, Baross u. 13. Dr. MOLNÁR, K, Veterinary Research Institute of the Hungarian Academy of Sciences Budapest, Hungária krt. 21.