Philippine Journal of Science 133 (1): 55-69, June 2004 ISSN 0031 - 7683

On a New of the Genus Stiles and Hassall, 1905 (Nematoda: ) from Bufo melanostictus Schneider, 1799 from Belur and Habra,West Bengal, India, With a Host-Parasite List

Mukul (Dutta) Sarkar and Buddhadeb Manna

Parasitology Research Unit Department of Zoology, University of Calcutta 35 Ballygunge Circular Road, Calcutta-700 019, India

The lungs of Bufo melanostictus Schneider, 1799 collected from West Bengal, India, were found to be infected with Rhabdias bulbicauda sp. nov., wisth the female specimen having a bulbiform caudal end.The description of the species is given. A host-parasite list of Rhabdias spp. and a comparative chart of close valid species of the genus Rhabdias is added.

Keywords: Rhabdias, lung , bulbiform caudal end, Bufo melanostictus, West Bengal, India.

During the course of a study on from parasites of vertebrates, Key No. 9 (Anderson and frogs and toads at Belur and Habra, West Bengal, Odile Bain, 1982) and Baylis (1936) were followed for India, specimens were recovered from the lungs of identification of the nematodes. Bufo melanostictus Schneider, 1799. These specimens are identified as a species under the genus Rhabdias Whenever the specimens were examined they Stiles and Hassall, 1905. On subsequent thorough were cleared in creosote (Beech Wood) oil. Before investigation they appeared to be new to science and restoring them into the 70% glycerine alcohol, the is described specimens were washed for about 4-5 minutes for two to three times in 70% acid alcohol to prevent darkening. All the measurements are in millimeter (mm) unless otherwise mentioned. Figures were drawn with the help of a Camera lucida. The Materials and Methods measurements mentioned in the text are the average Bufo melanostictus, the common Indian toad, were of 10 specimens studied. collected from its natural habitat, the damp, moist paddy fields and gardens at Belur, Howrah District and Habra, Materials examined North 24-Parganas District, West Bengal, India during 1996 to 2000. The nematodes after recovery from the 1. Holotype 1 female (Fig.1a, b, c. d ), paratype 4 lungs of freshly sacrificed toads were straight in 70% female – 24.7.98, 5 female − 13.5.2000; Host hot (about 60°C) alcohol, and then preserved in fresh Bufo melanostictus; location lung; locality Habra, 70% alcohol with a few drops of glycerine and kept North 24-Parganas District, West Bengal, India; with proper labelling. The CIH keys to the Coll. Mukul (Dutta) Sarkar.

55 Sarkar & Manna

2. Paratype 2 female − 11.11.96; Host Bufo Stiles & Hassall, 1905, were found to be present in melanostictus; location lung; locality Belur, the same lung in four toads in the ratio of 1:3, 1: 7, Howrah District, West Bengal, India; Coll. 2:2 and 4:1. The rest of the hosts were infected with Mukul (Dutta) Sarkar. R. bufonis (Table 2). The percentage of infection of R. Holotype and all the paratypes were deposited at bufonis was calculated in the present study as 22.90 the collection of Parasitology Laboratory, Department and intensity of infection as 4.55 and percentage of of Zoology, the University of Calcutta, 35 Ballygunge the present species R. bulbicauda sp. nov. as 2.54 Circular Road, Kolkata 700 019, India and intensity of infection as 3.14 (Table 2) only. The measurements of R. bufonis recovered in the present observation differ from previous descriptions and are Etymology presented in Table 1. This species is named as R. bulbicauda sp. nov. due to the bulbiform structure at the caudal end of the Male:Unknown body of the female Female : Body 12.24-12.8 long, 0.48 wide; nerve ring 0.16-0.17 from the anterior end; excretory pore Observation 0.192-0.208 from the head; oesophagus 0.64-0.88 long; During the study period (1996 – 2000) a total 275 cervical gland 0.4 long; vulva 1.84-1.92 from the head hosts were examined of which 70 were infected by end; tail bulbular, (1.12-1.92) x (0.96-1.76) in diameter this nematode. Of the infected hosts 7 were infected (Fig. 1, 2a, b and 5); eggs (0.080-0.096) x (0.032-0.048) with the present species of the genus Rhabdias and in diameter, embryonated (Table-1). the rest 63 were infected with R. bufonis (Table 1). The female nematodes remain embedded in the During collection two species of nematodes, the present lung alveoli (Figures. 2, 3). The caudal end has a species along with (Schrank, 1788) button-like deep brown bulb which remains on the

Table 1. Morphometric variations of closely related species of Rhabdias spp. Stiles and Hassall, 1905 and the present species (measurements in mm).

Fotedar’s (1965) Rbabdias bufonis Rbabdias ranae Gupta’s (1960) Rbabdias bulbicauda Rhabdias bufonis Rbabdias escheri (Schrank, 1788) Stiles Walton, 1929 Rbabdias ranae sp. nov. in the present (Schrank, 1788) Stiles Baer, 1930 and Hassall,1905 in the in the present Walton, 1929 observation and Hassall, 1905 present observation observation Bangladesh, Distribution Kashmir, India South India West Bengal, India West Bengal, India West Bengal, India Asia Peters, Rana tigrina Bufo viridis Rana tigrina 1879; Uraeotyphlus Bufo melanostictus Daudin, 1803 and Bufo melanostictus Host Laurenti1870 Daudin, 1803 oxyurus Schneider, 1799 Rana hexadactyla Schneider,1799 (Dumeril and Bibron) Lesson,1834

Location Lungs Lungs Body cavity Lungs Lungs Lungs

Characters / Body parts Female Female Female Female Female Female 12.24-12.8 1 Length of body 4.5-12.5 5.54-7.6 5-6 12.41-16.73 1.88-9.95

2 Breadth of body 0.2-0.4 0.3-0.38 0.25-0.26 0.32-0.64 0.11-0.41 0.40-0.48 0.5 x 0.05-0.07 3 Length of oesophagus 0.5 0.34-0.37 0.64-0.89 0.14-0.48 0.64-0.88 (Diameter) Distance of nerve ring from 4 - 0.17-0.19 - 0.05-0.32 0.03-0.176 0.16-0.17 anterior end 5 Length of buccal cavity 0.024-0.027 - 0.015 Minute 0.03 0.016-0.024 Distance of excretory pore 6 - - - Non traceable 0.12-0.28 0.192-0.208 from anterior end a) Position of vulva from 7 - - 0.15 7.84-12.08 1.15-5.6 1.84-1.92 anterior end b) Position of vulva from - 2.6-3.2 - - - - posterior end (0.064-0.128) x (0.03-0.04) x (0.04- (0.080-0.096) x (0.032- 8 Diameter of egg 0.115 x 0.06 0.1 x 0.55-0.65 No eggs observed (0.048-0.064) 0.14) 0.048) Bulbiform 9 Length of tail - 0.21-0.39 0.12 0.19-0.4 0.09-0.54

10. Diameter of bulbular tail x x x x x (1.12-1.92) x (0.96-1.76)

56 Rhabdias Infection on Lungs Bufo melanostictus

Table 2. Percentage and intensity of infection of Rhabdias spp. (Schrank, 1788) Stiles and Hassall, 1905 infecting Bufo melanostictus Schneider, 1799 in different seasons of the year No of Rhabdias No. of host No. of host Bufo No. of host No of bufonis (Schrank, infected by melanostic-tus infected by Percentage Intensity Rhabdias Percentage Intensity Seasons 1788) Stiles and Rhabdias Schneider, 1799 Rhabdias of infection of infection bulbicauda sp. Hassall, 1905 bulbicauda sp. of infection of infection examined bufonis nov. collected collected nov.

Winter (Dec-Jan- 34 15 59 1 2 Feb; S1)

Summer (March- 63 15 55 4 9 April-May; S2)

Rainy (June-July- 95 14 62 1 9 Aug.; S ) 22.90% 4.55 3 2.54% 3.14

Autumn (Sept-Oct- 83 19 111 1 2 Nov; S4)

Total 275 63 287 7 22

d 0.3 mm

a

c 0.4 mm

b Figure 2. Photomicrograph of a dissected Bufo melanostictus infected with R. bulbicauda in its . Rhabdias bulbicauda n. sp. Camera lucida drawing (Holotype); Figure 1 right lung, black globular head on the lung surface - anterior portion of female worm, - vulval region, - caudal bulb, a b c (arrow marking); (natural size). and d - egg

57 Sarkar & Manna

Figure 4. R. bulbicauda n. sp.; Photomicrograph posterior caudal end of the femal x40.

Figure 3. Photomicrograph with R. bulbicauda (deep brown pin heads); on the right side are two separate whole parasites (natural size). surface of the lung while the rest of the body remains Discussion coiled inside the lung alveoli surrounding the capillaries (Fig.3, 4). Surrounding the parasites the lung alveoli remain blackish red .This bulging bulb structure in Generic Diagnosis the juvenile or subadult stage of the specimen is large The body is smooth and unstriated, mouth terminal and gradually decreases in size as the worm grows to and surrounded by 6 small and insignificant lips. Each maturity (Figures 1,2,3,4). Some haemorrhagic spots of the lateral lips bears a lateral papilla. Rhabdias are seen around the nematodes on the surface of the with a cup-shaped buccal cavity. The oesophagus lungs. Both the lungs and sometimes one lung remain short, cylindrical club-shaped ending in a bulb. The infected. Most of the parasites come out automatically oesophageal part of the body is thinner than the rest of when kept in normal saline while a few still remain the body. Two large cervical gland present with nuclei coiled within the lungs. The gut of this nematode near the posterior end. Anus terminal; Rectal gland not always remain filled up with blood and thus they are visible. The vulva is in the anterior half of the body. Uteri blood feeder. opposed, didelphic, ovaries reflexed, ovoviviparous. The eggs in the uteri near the vagina are in the morula These parasites are recovered during summer stage. Adult females (parasitic form) in the lungs of (March-April-May, S2), rainy season (June-July-August, and reptiles. S3) and Autumn (September-October-November, S4) and only in one toad in the winter season (December- January- February, S1). Remarks Order : Rhabditida Stiles and Hassall (1905) established the genus Superfamily : Rhabditoidea Travassos, 1920 Rhabdias and included the type species Rhabdias Family : Railliet, 1916 bufonis (Schrank, 1788) from American Bufo sp. Its Genus : Rhabdias Stiles & Hassall , 1905 biology constantly attracted the attention of researchers Rhabdias bulbicauda sp. nov. because of the peculiarities of its development. The parasitic females of different species of this genus on the basis of which descriptions were mainly compiled are similar to each other. Linstow (1906), Goodey

58 Rhabdias Infection on Lungs Bufo melanostictus

(1924a), Travassos (1926) and Semenow (1929) added The present species is more closer in its some new species under this genus. Travassos (1930) measurements to R. bufonis, R. escheri and R. ranae. in his review of the genus assigned 15 species to it. The most common and well studied species is R. Liu (1934) listed 21 species for the genus Rhabdias. bufonis (Schrank, 1788). This species is very common This genus contain two generations; one free living in the lungs,and in rare cases in the body cavity, where microscopic form with a fairly stout body where the it is reported to harbour in competition (antagonism) with sexes are separate, and another parasitic generation, the trematode Haplometra cylindracea although the two much larger than the free living generation consisting species rarely occur together (Smyth and Smyth, 1980). of only “female” slender forms (Baylis, 1936). In the present observation, both Rhabdias bufonis and the present species are recorded in the lung of the In this present study, the present species of Rhabdias same host although very few in number (Table 2). The is recorded from Bufo melanostictus in summer, rainy number of R. bufonis is always higher than the present and autumn and rarely in winter seasons from Habra, species. Another species R. ranae Walton, 1929 is also North 24-Parganas District and Belur in Howrah District of well studied and well distributed all over the world in West Bengal, India. In winter the toad Bufo melanostictus frogs, toad and reptiles (Tables - 3, 4 & 5). R. bufonis, undergoes hibernation and very rarely comes out so the R. escheri and R. ranae, in the present observation incidence of infection is also rare. differ in measurements from previous records (Table - 1)

Table 3. Host-parasite list of Bufo spp. with Rhabdias spp. Stiles and Hassall, 1905. Sl.No Host Parasite Locality Reference 1 Bufo viridis Rhabdias bufonis Kashmir, India Fotedar, 1965 R. globocephala (Syn. of R. bufonis) “ “ ” Lublin area, Poland Kolendo, 1959 ” Tashkent, Uzbekistan,USSR Vashetko and Siddikov, 1999. ” Bursa and Büjükdöllük marsh, Yildirimhan, 1993. Edirne, Turkey Soviet Union & W.Europe Schneider, 1886 R. rubrovenosa R. rotundata Corfu (Europe) Linstow, 1906 R. microoris Russia Semenow, 1929. 2 Bufo marinus R. fuelleborni Bermuda, Atlantic Ocean Goldberg and Bursey, 1995. R. sphaerocephala Australia Speare, 1990. ” South America Kloss, 1972 ” Mexico R. hermaphrodita South America Goodey,1924 R. sphaerocephala (Syn. R. fuelleborni) Kloss, 1972 R. elegans Syn. R. fuelleborni) Kloss, 1974. R. sphaerocephala Bermuda Islands Williams, 1960. R. fuelleborni ” Linzey et al., 1998. R. elegans Brenes and Bravo Hollis, 1959. R. hermaphrodita Goodey, 1998 R. sphaerocephala R. fuelleborni Costa Rica, Central America R. sphaerocephala ” Veracruz, Mexico Rhabdias cf. Hylae North Queensland, Australia Barton, 1998. continue on next page. . .

59 Sarkar & Manna

Table 3 continuation . . . R. fuelleborni Pacific-coast of Jalisco, Mexico Galicia-Guerrero et al., 2000. R. fuelleborni Brazil, Salvador Travassos, 1926,. Goodey, 1924. Bufo regularis R. bufonis South Western Nigeria Aisien et al., 2001 3 Bufo bufo Larva of R. bufonis Europe Goater and Ward, 1992, Syn. B. asiaticus R. sensustricto Central Europe Goater, 1994 B. cinereus R. dossei Soviet Union Hartwick, 1972 B. terrestris R. microoris Florida, USA Semenow, 1929 B. vulgaris R. ranae Walton, 1929 R. bufonis Hanover, Germany Schmidt and Enigk, 1972. ” Bursa, Turkey Yildirimhan et al., 1997. R. sphaerocephala Kiev region, Ukraine; Kuz’min, 1997. Great Britain to South Western Russia Bufo bufo (Juvenile) R. bufonis Switzerland Goater and Ward, 1992. Bufo bufo asiaticus R. bicornis China Liu, 1934. R. microoris Russia Semenow, 1929. 4 Bufo debilis R. americanus New Mexico Goldberg et al., 1995. 5 Bufo cognatus R. americanus ” Goldberg et al., 1995. 6 Bufo alvarius R. americanus Southern Arizona, USA Goldberg and Bursey, 1991. 7 Bufo typhonius R. androgyna Belem (Para), Brazil Kloss, 1971. 8 Bufo crucifer R.hermaphrodita Brazil Kloss, 1971. 9 Bufo horribilis R.sphaerocephala Veracruz, Mexico Caballero, 1974. ” Guatemala Travassos, 1926. ” Chiapas Goodey, 1924. R. fiilleborni Guatemala Travassos, 1926. 10 Bufo americanus R. americanus Canada Baker, M.R. 1979a and b, 11 Bufo marmoreus R. fuelleborni Pacific coast of Jalisco, Mexico Galicia-Guerrero et al., 2000. 12 Bufo arenarum R. elegans Salta Province, Argentina Ramirez et al., 1979. and Seuldo and Ramirez, 1976. ” La plata, Argentina Gutierrez, 1945. 13 Bufo boreas Rhabdias sp. Southern California., USA Koller and Gaudin, 1976. Hyla regilla 14 Bufo vulgaris japonica R. bufonis Japan Miura, 1954. R. rubrovenosa Soviet Union Schneider,1886 R. incerta Japan Wilkie, 1930. R. shpaerocephala Europe Goodey, 1924. 15 Bufo melanostictus R. bufonis Garhwal Himalaya, India Chopra et al., 1991, 1992. R. brachylaimus Siam (Thailand) Linstow, 1903. 16 Bufo retiformis R. americanus Arizona, USA Goldberg et al., 1996a. 17 Bufo woodhousi R. americanus South Western and central Arizona Goldberg et al., 1996b. 18 Bufo microscaphus ” ” ” 19 Bufo hemiophrys R. americanus Alberta, Canada Bursey and Goldberg, 1998. 20 Bufo terrestris R. ranae Canada Leidy, 1851 R. entomelas U.S.A. Walton,1929 Canada Travassos, 1930. continue on next page. . .

60 Rhabdias Infection on Lungs Bufo melanostictus

Table 3 continuation . . .

21 Bufo fowleri ” Canada ” 22 Bufo cinereus R. rubrovenosa Europe Schneider, 1866. 23 Bufo houstonensis R. ranae Houston Thomas et al., 1984. 24 Bufo spp. R. bufonis Cairo Egypt Moravec et al., 1987. R. elegans Cuba Barus, 1973. R. fuelleborni Brazil Kloss, 1971. R. elegans R.sphaerocephala Rhabdias bufonis Sensu lato Central Europe Hartwick, 1972.

Table 4. Host-parasite list of Rana spp. with Rhabdias spp. Stiles and Hassall, 1905. Sl.No Host Parasite Locality Reference 1 Rana tigrina Rhabdias ranae Bangladesh Gupta, 1960. 2 Rana temporaria R. bufonis ? Lees, 1962. Southern Sweden Cedhagen, 1988. R. montana Ornativentris, Japan Yamaguti, 1954. R. bufonis Lithuania Gaizhauskene and Getsevichyute, 1970. Shores of lake Drukshyai, USSR Getsevichyute and Mitskevichene, 1982. R. montana Mount Ontake Japan Yamaguti, 1954. R.bufonis Leningrad, USSR Markov, 1955. Smyth and Smyth 1980. ” ? R. microoris Russia Semenow, 1929. 3 Rana esculenta R. bufonis ? Smyth and Smyth 1980. 4 Rana pipiens R. ranae USA Walton, 1929 Smyth and Smyth 1980. Goldberg et al., 2001, 5 Froglets of Rana pipiens R. ranae From Foggy Bottom Marsh in Southern Gillilland and Muzzall, 1999. Michigan, U.S.A. 6 Rana sylvatica R. ranae Southern Michigan Muzzall and Peebles 1991. R. ranae Guelph,Ontario,Canada Baker, 1979a,b. Leidy, 1851 R. entomelas Canada, U.S.A. Travassos, 1930. 7 Pseudacris c. crucifer R. ranae Southern Michigan Muzzall and Peebles, 1991. 8 Rana ridibunda R. bufonis Warszowa, Poland Kuc and Sulgostowska,1988. R. bufonis Kazakhstan Soboleva, 1975. Rana esculenta japonica R. bufonis Bursa and Edirne regions of Turkey, Asia Yildirimhan et al., 1996 and 1997. Japan and China Wilkie, 1930 R. incerta 9 Rana arvalis ” Irtysh river basin, Siberia, Russia Vakker, 1990. ” Southern Sweden Cedhagen, 1988. 10 Rana aurora R. joaquinensis Vancouver Island, Canada Moravec, 1984. R. joaquinensis California Ingles, 1936. 11 Rana daemeli R. australiensis Australia Moravec and Sey, 1990. 12 Rana cancrivora R. multiproles Malaya Yuen, 1965. continue on next page. . .

61 Sarkar & Manna

Table 4 continuation . . . R. nipponica R. brachylaimus 13 Rana bufonis R.bufonis Portugal Oliveira et al., 1972. 14 Rana mascarenienses R. madagascariensis Madagascar Chabaud et al, 1961. 15 Rana adenopleura R. nipponica Meihua Mountain Nature, Reserve & Wang Puqin et al.,1992. surrounding area, China R. bicornis R. bufonis 16 Rana chiricahunsis R. ranae Arizona Goldberg et al., 1998. 17 Rana clamitans R. ranae Ohio, U.S.A. Bursey and De Wolf, 1998. 18 Rana tatahumarae R. ranae Canada, U.S.A. Leidy, 1851 Travassos, 1930 Bursey and Goldberg, 2001 Mexico 19 Rana blairi ” USA Goldberg et al., 2000 20 Rana plancyi R. incerta China, Japan Wilkie, 1930 21 Rana perezi R. bufonis In Sierrade, gudar, Part of the sistema Galeano et al., 1996. Iberico in North-east Spain 22 Rana rugosa R. nipponica Japan, China Yamaguti, 1935. 23 Rana grylio ” ” Walton, 1929. 24 Rana nigromaculata ” China Yamaguti, 1935. R . incerta China and Japan Wilkie, 1930. 25 Rana guntheri R. nipponica ” Yamaguti,1935 26 Rana limnocharis ” ” ” 27 Rana Palustris R. ranae U.S.A. Leidy, 1851, Travassos,1930. R . entomelas Canada ” 28 Rana catesbiana R. nipponica China, Japan Walton,1929 R.entomelas Canada Travassos, 1930. 29 Rana halecina ” ” Travassos, 1930. 30 ” R. entomelas U.S.A. Leidy, 1851, Dujardin,1845. 31 Rana spherocephala ” Canada Leidy, 1851, Travassos, 1930. 32 Rana rugolosa R. nipponica Hanoi, Vietnam Moravec and Sey, 1985,1990 33 Rana sp. R. microoris Russia Skarbilovich, 1950. R. füelleborni Guatemala Travassos, 1926. R. incerta China Liu, 1934. R. rubrovenosa Europe Schneider, 1866 34 Frog tadpoles R.ranae Canada Baker, 1979. Amphibians R. americanus Southern Ontario, Canada Baker, 1978. R. fuscovenosa R. ranae R. horriguchii R. incerta Japan Matsuo et al.,2001 ” ” 35 Spring peepers R. ranae Wisconsin (USA) Yoder and Coggnis, 1996

62 Rhabdias Infection on Lungs Bufo melanostictus

Table 5. A list of the reptilian hosts with nematode parasite Rhabdias spp. Sl.No Host Parasite Locality Reference 1 Naja nivea R. fuscovenosa South Africa Goodey, 1924 2 Naja sp. Rhabdias annulosa China Hsu, 1933 3 Drymobius bifossatus R. ophidia London Zoo Goodey, 1924 4 Chamaeleonis sp. R. chamaeleonis Tropical Africa Skrjabin, 1916 R. gamellipara ? Chabaud et.al.,1961 5 Anguis fragilis R. dujardini ? Maupas and Seurat, 1916 R. entomelas ? Dujardin, 1845 6 Zaocys dhumnades R. annulosa China Hsu,1933 7 Holarchus spp. R. annulosa China Hsu,1933 8 Lampropeltis getulus R. eustreptos (MacCallum, 1921) Florida (U.S.A.) Chitwood, 1934 9 Tropidonotus natrix R. fuscovenosa Europe Railliet,1899 R. fuscovenosa Sicily (Europe) Rizzo, 1902 Syn. of R. fuscovenosa var. catanensis 10 Natrix sipedon R. fuscovenosa China Chitwood, 1933 (Syn. of R. fuscovenosa var. catanensis) 11 N. tigrina *R. horigutii Japan Yamaguti,1943 12 N. tigrina laerates Rhabdias sp. China (Nanking) Lee, 1934

R. ophidia China Goodey, 1924 13 Natrix tringa Rhabdias sp. ? Liu, 1934 14 Natrix tessellata R. fuscovenosus Kazakhastan Soboleva, 1975 15 N. natrix ” ” Soboleva, 1975 R. bufonis Cairo, Egypt (Africa) Moravec et al., 1987 R. americanus Southern Ontario, Canada Baker, 1978 R. ranae R. fuscovenosus R. eustriptos 16 N. fasciatus picti-ventris R. fuscovenosa var. catanensis North America (Florida) Rizzo, 1902 17 Agkistrodon halys R. fuscovenosa var. brecaudata China (Asia) Chu, 1936 Hsu and Hoeppli,1931 brevicaudatus Syn. R. fuscovenosa 18 A. bilineatus R. vellardii Guatamala (South America) Pereira, 1928 19 Ancistrodon halys R. fuscovenosa ? Railliet, 1899 20 Sepedon haemachata R. vellardii South Africa Goodey, 1924 21 Agkistrodon halys R. fuscovenosa China Goodey, 1924 brevicaudatus 22 Ancistrodon halys R. fuscovenosa ? Railliet, 1899 23 Sepedon haemachata R. vellardii South Africa Goodey, 1924 24 Bitis arietans R. fuscovenosa South Africa Goodey, 1924 25 Coluber viridiflavus R. fuscovenosa Catania, Sicily (Europe) Rizzo, 1902 (Syn. of R. fuscovenosa var catanensis) 26 Coluber sp. R. fuscovenosa U. S. A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 27 Coluber leopardinus R. ophidia London Zoo Goodey, 1924 28 Thamnophis sirtalis R. fuscovenosa China Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) North America (Florida) Rizzo, 1902 continue on next page. . .

63 Sarkar & Manna

Table 5 continuation . . . 29 Thamnophis sp. R. fuscovenosa U.S.A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 30 Storeria sp. R. fuscovenosa U.S.A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 31 Lampropeltis sp. R. fuscovenosa U.S.A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 32 Elaphe sp. R. fuscovenosa U.S.A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 33 Liopeltis sp. R. fuscovenosa U.S.A. Chitwood, 1933 (Syn. of R. fuscovenosa var catanensis) 34 Green snake R. fuscovenosa var. brevicauda China Chu, 1936; Hsu et; Hoeppli, 1931 35 Rhadinaea merremi R. labiata Brazil Pereira, 1927 36 Heterodon platyrhinus R. serpenticola (Linstow, 1904) North America; Germany Yamaguti, 1961 37 Philodryas schotti R. vellardii Brazil Pereira, 1928 38 Oxyrrhopus trigeminus R. vellardii Brazil Pereira, 1928 39 Heterodon sp. R. vellardii Texas Pereira, 1928 40 Storeria sp. R. vellardii Texas Pereira, 1928 41 Potomophis sp. R. vellardii Texas Pereira, 1928 42 Thamnophis sp. R. vellardii Texas Pereira, 1928 43 Ophibolus getulus R. eustreptos ? MacCallum, 1921 44 ” R. incerta Osaka Municipal Tennoji Zoo (Japan) Matsuo et al., 2001 45 Reptiles Rhabdis horiguchii ” ” *Yamaguti (1943) proposed its name as Ophiorhabdias sp. and these differences are considered as intra specific bufonis is 12.41−16.73 long and R. ranae is 1.88-9.95, variations. R. bufonis has been reported from Europe, while the present species is 12.24 − 12.80. Similarly Asia and North America (Skrjabin, 1984), Portugal other various body measurements also differ from that (Oliveira et al., 1972), West Europe (Hartwick, 1972), in the present species and is given in Table 1. Yugoslavia (Hristovski and Lees, 1973), Saudi Arabia (Nasher, 1979), Egypt (Moravec, et al., 1987) China From the present observation, this species under (Wang Puqin et al.,1992), Garhwal, India (Chopra discussion is recognised as new to science and hence et al.,1992) and Bangladesh (Gupta, 1960). the authors suggest its name as Rhabdias bulbicauda sp. nov. considering its bulbular caudal end in the The R. ranae was originally described by Walton female parasitic form in the lungs of B. melanostictus. (1929) for 65 adults from the lungs of Rana pipiens and Rana palustris and 21 larval forms from the The present species appears to be pathogenic as intestine and coelomic mesenteries of R. pipiens, R. blood clots and some damage tissue in the lung alveoli palustris and Acris gryllus from North American states are observed around the parasite. Similar observation and subsequently, Morrison (1967a, b) recorded it is also available from Chopra et al. (1991, 1992) in in Oklahoma, Ashton and Rabalais (1978) in Ohio, R. bufonis infection in the lungs of B. melanostictus Baker (1978) in Ontario, Williams and Taft (1980) in which causes severe damage in the lung capillary Wisconsin.In the present study Rhabdias ranae is network during its active movement in this parasite also recorded from Rana tigrina and R. hexadactyla species is recorded for the first time in the lungs of (Table 4). Bufo melanostictus, West Bengal, India, although in a very low percentage. The species under discussion differs from all the valid species in its caudal bulbular structure in the female specimen and in all other morphmetric measurements and so far no record of such nematode is available. The Acknowledgments described species in the present study, does not agree with any of the known and well described species of The author is grateful to the Head, Department of this genus in having a bulbular caudal end. The present Zoology, Calcutta University for providing necessary species also differs in various body measurements. R. laboratory facilities and also to Sri S. R. Dey Sarkar,

64 Rhabdias Infection on Lungs Bufo melanostictus

Helminthology Department, Zoological Survey of India, and Strongyloidea). London : Taylor and Francis, Calcutta for his constant inspiration and cooperation in 408pp. the identification of the nematode parasite. The author Bogoyavlenskii Yu K, Goshkheteliani IS, Sharipova also wishes to thank and express indebtedness to her AA & Shchukin PI. 1975. The micromorphology of parents Sri Padma Lochan Dutta and Smt. Basana some helminths and the variations of the defense Rani Dutta, and to sisters Smt. Purnima Dutta, Smt. response of the infected host. II. Fine structure of Priti Dutta and husband Dr. Sovan Sarkar for their the integument of the lung nematodes, Syngamus assistance in collecting the hosts in the field and also trachea (Montagu, 1811) Chapin, 1925 and for financial assistance and encouragement. Rhabdias bufonis (Schrank, 1788) In: Nekotorye voprosy biologii razvitiya zhivotnykh. Vyp. 1. Tbilisi USSR; Izdatel’ stvo Tbilisskogo Universiteta (1975): 188−193. References Bolek MG & Coggins JR. 2000. Seasonal occurrence Aisien SO, Ugbo AD, Ilavbare AN & Ogunbor O. 2001. and community structure of helminth parasites Endoparasites of amphibians from South Western from the eastern American toad, Bufo americanus Nigeria. Acta Parasitologica. 46 : 299-305. americanus from southeastern Wisconsin, U.S.A. Anderson RC & Odile Bain. 1982. CIH keys to the Comparative Parasitology. 67 : 202-209. nematode parasites of vertebrates No.9. Keys to Brenes RR & Bravo Hollis M. 1959. Helmitos de la the genera of the super families Rhabditoidea, Republica de-costa Rica viii, Nematoda 2. Algunos Dioctophymatoidea, Trichinelloidea and nematodes de Bufo marinus marinus (L.) Y algunas Muspiceoidea. Anderson, R.C., Chabaud A.G., consideraciones sobre los generos oxysomatium Y- and Willmott, S.(Eds.). Common Wealth Institute of Aplectana. Revista de Biologia Tropical Universidad Helminthology, London 1−25. de Costa Rica, 7 : 35−55. Ashton AD & Rabalais FC. 1978. Helminth parasites of Bursey CR & Goldberg SR. 2001. Falcaustra lowei n. some anurans of north western Ohio. Proceedings sp. and other helminths from the Tarahumara frog, of the Helminthological Society of Washington, 45: Rana tarahumarae (Anura : Ranidae) from Sonora, 141−142. Mexico. Journal of Parasitology, 87: 340-344. Baer JG. 1930. Deux helminthes nouveaus parasites Bursey CR & De Wolf WF. 1998. 11 Helminths of the de Uraeotyphlus oxyurus (Gray), Gmnophione de frogs Rana catesbeiana, Rana clamitans, and Rana L’ Inde meridionale. Revue suisse de Zoologie, 37: palustris, from coshocton county, Ohio. Ohio Journal 43-52. of Science, 98: 28−29. Baker MR. 1978. Morphology and of Rhabdias Bursey CR & Goldberg SR. 1998. Helminths of the spp. (Nematoda : Rhabdiasidae) from reptiles and Canadian toad, Bufo hemiophrys (Amphibia : Anura) amphibians of Southern Ontario. Canadian Journal from Alberta, Canada. Journal of Parasitology, 84 : of Zoology, 56: 2127−2141. 617−618. Baker MR. 1979a. The free-living and parasitic Caballero Deloya J. 1974. A helminthological study of development of Rhabdias spp. (Nematoda : wild at the station of tropical biology, “Los Rhabdiasidae) in amphibians. Canadian Journal of Tuxtlas”, vera cruz. Nematodes I. Some parasitic Zoology, 57 : 161−178. nematodes in Bufo horribilis Wiegmann, 1833. Baker MR. 1979b. Seasonal population changes Universidad Nacional Autonama da Mexico, Serie in Rhabdias ranae Walton, 1929 (Nematoda: Zoologia 45 : 45−50. Rhabdiasidae) in Rana sylvatica of Ontario. Cedhagen T. 1988. Endoparasites in some Swedish Canadian Journal of Zoology, 57 : 179−183. amphibians. Acta Parasitologia Polonica 33: Barton DP. 1998. Dynamics of natural infections of 107−113. Rhabdias cf. hylae (Nematoda) in Bufo marinus Chabaud AG, Brygoo ER & Petter AJ. 1961. Description Amphibia in Australia. Parasitology, 117: 505−513. et caracteres biologiques de deux nouveaux Barus V. 1973. Nematodes parasitizing hosts of the Rhabdias malgaches. Annales de Parasitologie genus Bufo (Amphibia) in Cuba. Folia Parasitologica, Humaine et comparee. 36: 752-763. 20: 29−39. Chitwood BG. 1933. On some nematodes of the Baylis HA. 1936. The Fauna of British India, including Superfamily Rhabditoidea and their status as Ceylon and Burma. Nematoda vol 1. (Ascariodea parasites of reptiles and amphibians. Journal of the

65 Sarkar & Manna

Washington Academy of Sciences. Washington. Nauk Litovskoi SSR, Institute Zoologii i Parazitologii 23: 508-520. 20-21 [Ru]. Chitwood BG. 1934. Reports on the collections Gillilland MG & Muzzall PM. 1999. Helminths infecting obtaied by the first Johnson. Smith sonian deep. froglets of the northern leopard frog (Rana pipiens) Sea expedition to the puerto Rican deep. Two new from Foggy Bottom Marsh, Michigan. Journal of the nematodes. Smithsonian Miscellaneous Collections. Helminthological Society of Washington 66: 73−77. Washington. 91: 4 pp. Goater CP. 1994. Growth and survival of post Chopra AK, Singh N & Bhatt KC. 1991. Erythrocytic metamorphic toads. Interactions among larval changes in Bufo melanostictus naturally infected history, density and parasitism. Ecology 75 : with nematodes. Indian journal of Parasitology 15: 2264−2274. 111−112. Goater CP & Ward PI. 1992. Negative effects of Rhabdias Chopra AK, Singh N & Bhatt KC. 1992. Effect of bufonis (Nematoda) on the growth and survival of nematode infection on heart beat rate of Bufo toads (Bufo bufo). Oecologia 89: 161−165. melanostictus. Indian Journal of Helminthology 43: Goldberg SR, Bursey CR, Mckinnell RG & Tan IS. 156−158. 2001. Helminths of northern leopard frogs Rana Chopra AK, Singh N & Bhatt KC. 1992. Effect of pipiens (Ranidae) from North Dakota and South nematode infection on heart beat rate of Bufo Dakota. Western North American Naturalist. 61(2): melanostictus. Indian Journal of Helminthology. 248-251. 43(2): 156 - 158. Goldberg SR, Bursey CR & Platz J E. 2000. Helminths Chu TC. 1936. A review of the status of the reptitian of the plains leopard frog, Rana blairi (Ranidae). nematodes of the genus Rhabdias with a redescription South Western Naturalist. 45: 362-366. of Rhabdias fuscovenosa var. catanensis (Rizzo, Goldberg SR & Bursey CR. 1991. Helminths of three 1902) new rank. Journal of parasitology. Lancaster, toads, Bufo alvarius, Bufo cognatus (Bufonidae) and Pa. 22(2): 130-139. Scaphiopus couchii (Pelobatidae) from Southern Dujardin F. 1845. Histoire naturelle des helminthes ou Arizona. Journal of the Helminthological Society of vers intestinaux-Paris xvi + 654 + 15. Washington 58: 142−146. Fotedar DN. 1965. Rhabdias bufonis (Schrank, 1788) Goldberg SR, Bursey CR & Ramos I. 1995. The Stiles and Hassall, 1905 from the lungs of Bufo viridis component parasite community of three sympatric in Kashmir and notes on some species toad species. Journal of the Helminthological Society of the genus. Kashmir Science, 2: 20−26. of Washington 62: 57−61. Gaizhauskene I & Getsevichyute S. 1970. On Goldberg SR & Bursey CR. 1995. Helminth of an the parasite fauna of Rana temporaria in the introduced population of the gaint toad. Bufo marinus neighbourhood of Kaunas. Acta Parasitologica Anura : Bufonidae from Bermuda. Journal of the Lituanica, 10: 103−108. Helminthological Society of Washington 62: 64-67. Galeano M, Navarro P & Lluch J. 1996. Helminth fauna Goldberg SR, Bursey CR & Cheam H. 1998. Helminths of some amphibians and reptiles from the Spanish of two native frog species Rana chiricahuensis, Rana “Sistema Ib’erico mountains. Anales de Biologia 21 yavapaiensis and one introduced frog species (Rana (Biologia 10) : 23−30. catesbeiana) (Ranidae) from Arizona. Journal of Parasitology 84: 175−177. Galicia-Guerrero S, Bursey CR, Goldberg SR & Salgado- Maldonado G. 2000. Helminths of two sympatric Goldberg SR, Bursey CR, Sullivan BK & Truong QA. toad species, Bufo marinus (Linnaeus) and Bufo 1996a. Helminths of the Sonoran green toad, Bufo marmoreus Wiegmann, 1833 (Anura: Bufonidae) retiformis (Bufonidae) from Southern Arizona. Journal from Chamela, Jalisco, Mexico Comparative of the Helminthological Society of Washington 63: Parasitology 67: 129−133. 120−122. Getsevichyute SYu & Mitskevichene GP. 1982. [Parasite Goldberg SR, Bursey CR, Malmos KB, Sullivan BK & fauna of Rana temporaria from the shores of Lake Cheam H. 1996b. Helminths of the Southwestern Drukshyai]. In Aktual nye problemy parazitologii V toad, Bufo microscaphus, woodhouse’s toad, Pribaltike. Materialy K IX Nauchnokoordinat sionnoi Bufo woodhousii (Bufonidae) and their hybrids Konferentsii Po probleman parazitologii V Pribaltike, from Central Arizona. Great Basin Naturalist 56: 1-2 Iyulya 1982 g.) Vilnius, U.S.S.R.; Academiya 369−374.

66 Rhabdias Infection on Lungs Bufo melanostictus

Goodey, T. (1924a). On two new species of the nematode Koller RL & Gaudin AJ. 1976. An analysis of helminth genus Rhabdias. Journal of Helminthology. 2: infections in Bufo boreas (Amphibia : Bufonidae) 203−208. and Hyla regilla (Amphibia : Hylidae). Southwestern Naturalist. 21: 503−509. Goodey T. 1924b. The Anatomy and Life History of the Nematode Rhabdias fuscovenosa (Railliet) from Kuc Sulgostowska 1988. Helminth fauna of Rana the Grass snake Tropidonotus natrix. Journal of ridibunda Pallas, 1771 from Goclawski canal in Helminthology. 2: 51. Warszawa (Poland). Acta Parasitologica Polonica 33 : 101−105. Gupta SP. 1960. Nematode parasites of East- Pakistan VI. Amplicaecum cacopi. The landros sp., Kuz’min Yu I. 1997. Life-cycle and new data on the Rhabdias ranae, and Oswaldocruzia melanosticti distribution of Rhabdias sphaerocephala (Nematoda, sp. nov., from frogs. Canadian Journal of Zoology Rhabdiasidae). Vestnik Zoologii 31: 49−57. 38: 745−750. Lees E. 1962. The incidence of helminth parasites in a Gutierrez RO. 1945. Contribucion al.conocimiento de particular frog population. Parasitology, 52: 95−102. los nematodes, parasitos de anfibios argentinos. Leidy J. 1851. Description of new species of entozoa. Tesis-la plata No. 8: 37 pp. Proceedings of the Academy of Natural Sciences of Hartwick G. 1972. Uber Rhabdias bufonis (Schrank, Philadelphia 5: 155−156. 1788) und die Abtremmung Von Rhabdias dossei Linstow O Von. 1903. Parasiten, meistens Helminthen, nov. spec.(Nematoda Rhabdiasidae). Mitteilungen aus, siam. Archiv für mikroskopische Anatomie (und sus dem Zoologischem Museum in Berlin 48: Entwicklungs-mechanik). 62: 108−121. 401−414. Linstow O Von. 1906. Nematoden des Zoologischen Hristovski ND & Lees E. 1973. The helminth fauna Museums in Konigsberg. Archiv für Naturgeschichte. of Rana temporaria in relation to that of Europe Berlin 22: 249−258. generally. Acta Parasitologia Iugoslavica 4: 93−97. Linzey DW, Bursey CK & Linzey JB. 1998. Seasonal Hsu HF & Hoeppli RJ. 1931. Parasitic nematodes mostly occurrence of helminths of the giant toad Bufo from snakes collected in China. National Medical marinus (Amphibia: Bufonidae) in Bermuda. Journal Journal of China.Shanghai 17(4-5): 567-588. of the Helminthological Society of Washington 65: Hsu HR. 1933. On some parasitic nematodes collected 251-258. in China. Parasitology. Cambridge. 24(4): 512-541. Liu SC. 1934. On Rhabdias, a genus of parasitic Ingles LG. 1936. Worm parasites of California nematodes of Nanking. Sinensia 5: 164−172. Amphibia. Transaction of American microscopical MacCallum GA. 1921. Studies in helminthology.pt.3. Society 55: 73−92. Nematodes, Zoopathologica. 1(6) : 135-284. Khatoon N. 1967. Histochemical and ultrastructural Markov GS. 1955. Interspecific relationships in observations on Rhabdias bufonis [Abstract]. helminths co-existing in the lungs of grass frogs. Parasitology, 57: 7p. Dokladi Akademii Nauk SSSR 100: 1203-1205. Kloss GR. 1971. Some Rhabdias (Nematoda) of Bufo Matsuo K, Sumiya G, Oku Y & Kamiy M. 2001. Parasitic of Brazil. “Alguens Rhabdias (Nematoda) de Bufo no helminths from amphibians and reptiles in Osaka Brasil”. Published papeis Department of Zoological Municipal Tennoji zoo. Japanese Journal of Zoo and Society. Paulo 24: 1−52. Wildlife Medicine. 6(2): 35-44. Kloss GR. 1972. Rhabdias from Bufo of the marinus Maupas E & Seurat LG. 1916. Sur le méchanisme de 1’ group. A. study of sibling species (Nematoda accouplement chezles Nématodes C. U. Soc. Biol., Rhabditoidea). Thesis Universidade de Sao Paulo. vol. 79 p. 614. 90[+100] pp.[pt]. Micoletzky H. 1922. Archiv für Naturgeschichte, Barlin. Kloss GR. 1974. Rhabdias (Nematoda, Rhabditoidea) Abt. A, 87,245. In Baylis and Daubney, 1926. A from the marinus group of Bufo, A study of sibling synopsis of the families and genera of Nematoda. species. Arquivos de Zoologia, Sao Paulo 25: British Museum, London., P. 35. 61−120. Miura K. 1954. Studies on chemotherapy against Kolendo A. 1959. Helmintofauna ropuchy Zielonej hookworm disease on the effect of 1-bromo-β- Bufo viridis Laur. Wojewodztwa lubelskiego. Acta naphthol. Japanese Journal of Medical Science and Parasitologia Polonica, 7: 431−439. Biology 7: 265-273.

67 Sarkar & Manna

Moravec F. 1984. Some helminth parasites from amphibians Rizzo A. 1902. La fauna elmintologica dei rettili nella of Vancouver Island, Vestnik Ceskoslovenske provincia di calania. Archives de parasitologie. Paris. spolecnosti zoologicke, 48: 107-114. 6(1): 26-41. Moravec F & Sey O. 1985. Some nematode parasites of Runey MW. 1973. A study on gametogenesis and frogs (Rana spp) from North Viet Nam. Parasitologia fertilization in the heterogenic life cycle of Rhabdias Hungarica, 18: 63-77. ranae Walton, 1929, Dissertation Abstracts International, 338: 3497. In “Amphibian Nematodes Moravec F & Sey O. 1990. Some nematode parasites from South Asia” M.L. Sood, Indira Publishing of frogs from Papua New Guinea and Australia. House, USA pp 15. Acta Societalis Zoologicae Bohemoslovacae 54: 268-286. Schmidt U & Enigk K. 1972. Severe helminth infection in toads (Bufo bufo) . Deutsche Tierarzt liche Moravec F, Barus V & Rysavy B. 1987. Some Wochenschrift 79: 625-626. Parasitic nematodes, excluding Heterakidae and Pharyngodonidae from amphibians and reptiles in Schneider AF. 1866. Monographie der Nematoden, Egypt. Folia Parasitologica, 34: 255-267. Berlin, XIII + 357 PP. Morrison EO. 1967a. Mite and Lungworm infections Schrank FP. 1788. Verzeichniss der bisher hinlanglich in Acris crepitans from Southern Oklahoma, Texas bekannten Eingeweid ewiirmer, nebst einer Journal of Science, 19: 328-329. Abhandlung über ihre Anverwandt Schaften. München.116 PP. Morrison EO. 1967b. Rhabdias ranae infection in three species of Oklahoma anura, Southwestern Semenow VD. 1929. Eive neue Nematodenart Rhabdias Naturalist, 12: 335-336. microoris n.sp.-aus den Lungen Von Amphibian CtbI. Bakt.1.Orig. 114: 533-539. Muzzall PM & Peebles CR. 1991. Helminths of the wood frog Rana sylvatica and spring peeper, Pseudacris Shishov BA & Terenina NB. 1978. Study of egg laying c. crucifer, from Southern Michigan. Journal of in nematodes from different taxonomic groups. the Helminthological Society of Washington 58: Trudy Gel’ mintologicheskoi Laboratorii Nematody i 263−265. akantol sefaly, morfologiya Distemati Ka ekologiya i fiziologiya, 28: 115-121. Nasher AK. 1979. Helminth parasites of Bufo orientalis and Hyla arborea in Asia, Southwest, Saudi Arabia. Skarbilovich TS. 1950. A study of the biology of Capillaria Proceedings of the Saudi Biological Society 3: 265- mucronata (Molin, 1858) and the epizootology of 276. capillariosis of the urinary bladder of sable and mink. Trudy Vsesoiu. Inst Gelmint., 4: 27-33. Oliveira Rodrigues HDe, Rodrigues SS & Cristofaro R. 1972. Contributions to the study of nematodes Skrjabin KJ. 1916. Parasitic Trematodes and Nematodes from Rana esculenta L. in metropolitan Portugal. collected by the Expedition of Pro. V. Dogiel and I. Atas da Sociedade de Biologia do Rio de Janeiro, Sokolow in British East Africa and Uganda by Prof. V. 16: 21-26. Dogid and I. Sokolow in British East Afric. Scientific Results of the Zool. Exped to British east. Africa Pereira C. 1927. Fauna helmintologica dos ophideos and Ugadanga by Prof. V. Dogiel and 1. Sokolow brasileiros, Boletin Biologico, vol. 10. Sao. Paulo. in 1914, vol. 1. P.99. Pereira C. 1928. Fauna helmintologica dos ophideos Skrjabin KI. 1984. Key to parasitic nematodes Brasileiros, Rhabdias vellardi n. sp., Boletin Vol.4 Camallanata, Rhabdiata, Tylenchata, Biologico, vol. 11. Sao paulo. Trichocephalata, Deoctophymata and distribution Railliet A. 1899. Evolution sans hétérogonie d un of Parasitic nematodes in different hosts. Amerind angiostony de la couleuvre a collier. Compte rendu Publishing Co. Pvt. Ltd. New Delhi, Bombay, mensuel des séances de 1’ Académie des sciences Calcutta, New york, XI + 1097. coloniales. Paris, vol 129(26), p. 1271-1273. Smyth JD & Smyth MM. 1980. Frogs as host parasite Railliet A & Henry A. 1915. sur les nematodes du genres systems 1. London and Basingstoke U.K. The Goezia Zeder. Bulletin de la societi de pathologic MacMillan Press Ltd. IX-112pp. exotique. Paris. 8: 270-275. Soboleva TN. 1975. The helminth fauna of aquatic Ramirez VG, Sueldo C & Mesones RV. 1979. amphibians and reptiles of Kazakhstan. In Ekologiya Contributions on the parasites of Bufo arenarum Parazita vodneykh zhivotnykh. Alna. Ata. USSR. from Salta Province. Neotropica 25: 90. 186-192.

68 Rhabdias Infection on Lungs Bufo melanostictus

Soboleva TN. 1975. The helminth fauna of aquatic Williams D.D. and Taft. S.J. (1980). Helminth of amphibians and reptiles of Kazakhstan. In Ekologiya anurans from NW Wisconsin. Proceedings of the Parazitov vodnykh Zhivotnykh. Alna-Ata USSR; Helminthological Society of Washington, 47: 278. Izdatel stvo “Nauka” Kazakhskoi SSR. 186-192. Williams RW. 1960. Observations on the life history Speare R. 1990. A review of the diseases of the cave of Rhahdias sphaerocephala Goodey, 1924 from toad, Bufo marinus with comments on biological Bufo marinus L., in the Bermuda Islands. Journal of control. Australian wild life Research 7: 387-410. Helminthology, 34: 93-98. Stiles CW & Hassall A. 1905. The determination of Yamaguti S. 1935. Studies on the Helminth fauna of generic types and a list of roundworm genera with Japan Pt. 10. Amphibian nematodes. Japanese their original and type species, U.S. Dept. Agric., Journal of Zoology 6: 387-392. Bureau of Animal Industry, Bull. No. 79, 150 PP. Yamaguti S. 1954. Helminth fauna of Mt. Ontake, Part. 1. Sueldo C & Ramirez VG. 1976. The nematode Nematoda and Acanthocephala. Acta medica Okayama parasites of Bufo arenarum in the province of Salta. 8: 386-392. Neotropica 22: 105-106. Yamaguti S. 1943. Rhabdias (Ophiorhabdias) horigutti Thomas RA, Nadler SA & Jagers WL. 1984. Helminth n. subg. n. sp. (Nematoda) from the lung of a parasites of endangered Houston toad, Bufo Japanese snake, Natrix tigrina. Annotationes houstonensis Sanders, 1953 (Amphibia, Bufonidae). Zoolgicae Japonensis. Tokyo. 22(1) : 8-10. Journal of Parasitology, 70: 1012-1013. Yamaguti S. 1961. R. Serpenticola (Linstow,1904) in Travassos L. 1926. Entwick lung des Rhabdias Heterodon platyrhinus from Systema Helminthum fülleborni, n. sp. Archiv für schiffs u. Tropenhygiene, by Satya Yamaguti vol. 111, the Nematodes unter bes. Ber. d. Pathologie, u. therapie, Leipzig of vertebrates part 1. Pg. 122. Published by 30: 594-602. Interscience Publishers, Inc. New York and Interscience Publishers Ltd. London. Travassos L. 1930. Pesquizas helminthologicas realizadas em Hamburgo, VII, Notas Sobreos Yildirimhan HS. 1993. Researches on parasitic helminths Rhabdias oidea Railliet, 1916 (Nematoda). of Bufo viridis Laurenti , 1768 (Anura; Amphibia). Memorias do Instituto Oswaldo Cruz, Rio de Janeiro In Parazitik helmintleri, üzerine, arastirmala. Turkish 24: 161-181. Journal of Zoology 23 (Suppl): 177-195. Vakker VG. 1990. Separation and overlapping of Yildirimhan HS, Oguz, MC & Ugurtas IH. 1997. spatial temporal niches in imaginal forms of five An investigation of nematodes of tailless frogs helminth species in populations of Rana arvalis in (Rana ridibunda, Bufo bufo, Pelobates syriacus the central Irtysh basin. In Evolyutsiya Parazitov. collected from the Bursa regions. [Bursa ve Materialy Pervogovesoyuznogo simpoziuma sevresinden yakalanan bazi Kuyruksuz Kurba galarin (Tol’yatti, 16-19 Oktyabrya). Tol’yatti, Russia; (Rana ridibunda, Bufo bufo, Pelobates Syriacus) Institut Ekologii volzhskogo Basseina AN SSSR nematodlari üzerine bir arastirma]. Hacettepe. Fen (1991) 83-88 [Ru] Pavlodar Pedagogic Institute, ve Muhendislik Bilmleri, Dergisi seri A 18: 45-58. Pavlodar, Russia. Yildirimhan HS, Ugurtas IH & Altunel FN. 1996. An Vashetko EV & Siddikov BH. 1999. The effect of the investigation of helminths of Rana ridibunda Pallas, ecology of toads on the distribution of helminths. 1771 (marsh frogs). Rana ridibunda Pallas, 1771 Turkish Journal of Zoology 23:107-110. (Ova Kurbagasi) nin helmint leri üzerinde bir arastirma. Türkiye Parazitoloji Dergisi 20: 113-130. Walton AC. 1929. Studies on some nematodes of Northern american frogs. Journal of Parasitology Yoder HR & Coggins JR. 1996. Helminth communities 15: 227-240. in the northern spring peeper, Pseudacris C. Crucifer wied, and the wood frog, Rana sylvatica Wang Puqin, Wang Yanyin, Zhao Yuru, Yain Ruliu and Le Conte, from Southeastern Wisconsin . Journal Wang Shaoping, (1992). The parasitic helminths of the Helminthological Society of Washington 63: of vertebrates from Meihua Mountain Nature 211-214. reserve and adjacent area. Wuyi Science Journal 9: 31-48. Yuen PH. 1965. Some studies on the taxonomy and development of some rhabditoid and cosmocercoid Wilkie JS. 1930. Some parasitic nematodes from nematodes from Malayan amphibians. Zoologischer Japanese amphibia. Annals and Magazine of Natural Anzeiger 174: 275-298. History 6: 606-614.

69