Brazilian Journal of Biological Sciences, 2018, v. 5, No. 11, p. 747-756. ISSN 2358-2731 https://doi.org/10.21472/bjbs.051112
Digenean parasites of the water skipper Euphlyctis cyanophlyctis (Schneider, 1799) (Anura: Dicroglossidae) of the South Western Ghats, India
Shinad Keloth and Prasadan Puthanpurayil Kandambeth*
Ecological Parasitology and Tropical Biodiversity Laboratory. Department of Zoology. Kannur University. Mananthavady Campus. Wayanad- 670645. Kerala. India. *Email: [email protected].
Abstract. Five species of digenean parasites, Diplodiscus mehrai, Tremiorchis ranarum, Halipegus mehransis, Ganeo glottoides and Received Ganeo tigrinum, of the frog Euphlyctis cyanophlyctis (Schneider, September 26, 2018 1799) (Anura: Dicroglossidae) from the Wayanad Region of the South Western Ghats are reported in this paper. Multiple Accepted November 11, 2018 infections were also recorded during the study. Prevalence of infection of D. mehrai, T. ranarum, H. mehransis, G. glottoides and Released G. tigrinum were 12%, 8%, 2%, 31% and 8%, respectively, and December 31, 2018 the intensity of infection were 1.7, 34.4, 2, 4.5 and 2.9, respectively. Full Text Article
Keywords: Digenean parasites; Frog; Euphlyctis cyanophlyctis; Western Ghats; Prevalence.
0000-0002-3876-9697 Shinad Keloth 0000-0001-7228-8435 Prasadan Puthanpurayil Kandambeth
Introduction investigations, including those by Mehra and Negi (1926a, b, l928), Bhalerao Amphibians, particularly (1926, 1936a, b, c, 1937), Srivastava anurans, harbour a variety of adult and (1933a, b, 1934a, b), Pande (1937), larval trematodes involving freshwater Chauhan (1954), Gupta and Agrawal gastropods as first intermediate hosts in (1966, 1967), Pandey (1968, 1969a, b, their life-cycles (Duda and Verma, 1996). 1981), Gupta (1970, 1977), Mukherjee The trematode fauna of amphibians of and Ghosh (1970, 1972), Singh (1977) India has been the subject of numerous Janardanan et al. (1987), Janardanan and
ISSN 2358-2731/BJBS-2018-0065/5/11/12/747 Braz. J. Biol. Sci. http://revista.rebibio.net 748 Keloth and Kandambeth
Prasadan (1991), Brinesh and Chooralmala, Chundel, Ammana, Janardanan (2014) and Shinad and Karappuzha Dam, Kavummandham, Prasadan (2017a, b, 2018a, b). Singh Makkimala, Ondayangadi, Pakkam, (1977) made the first contribution to the Panamaram, Payyampally, Peechangode, trematode fauna of amphibians in Kerala. Pulpally, Thalappuzha and Wayanad Later Janardanan et al. (1987) recorded District. Pleurogenoides ovatus Rao, 1977 from Period of collection: January Rana tigrina (Hoplobatracus tigerinus) 2016 to October 2017. and later Janardanan and Prasadan (1991) elucidated its life cycle. The life Prevalence and intensity of cycle of a new species P. infection Malampuzhaensis was established by Prevalence and intensity of Brinesh and Janardanan (2014). Recently infection were measured following Bush four new species of digenetic trematodes et al. (1997). from amphibian hosts were reported One hundred specimens of E. from Western Ghats by Shinad and cyanophlyctis collected during the period Prasadan (2017a, b, 2018a, b). from January 2016 to October 2017 from The water skipper Euphlyctis various water bodies using sweep hand cyanophlyctis (Schneider, 1799) (Anura: net were brought to the Laboratory, Dicroglossidae) inhabits the maintained in cement cisterns and fed pools/standing waters in the plains and them occasionally with insects. The sub-mountainous areas of the Western specimens were narcotized with Ghats. It is widely distributed throughout chloroform, dissected, their skins were South Asia (Frost, 2014). Despite its removed, and the muscle tissues were common occurrence in different types of macerated to detect the presence of freshwater bodies, the parasite fauna had metacercariae. Internal organs were also not been a subject of any in depth study. dissected out from each frog, placed in During our studies on the digenean separate Petri dishes containing 0.75% parasites of frogs of the Western Ghats, saline, macerated and examined under Wayanad Region, an analysis was made the stereozoom microscope. Adults, on the species composition of digenean when present, were carefully removed, parasites of E. cyanophlyctis. This paper transferred to 0.75% saline in separate deals with the digenean parasites found watch glasses and studied under Nikon in E. cyanophlyctis of the Western Ghats, ECLIPSE Ni-U phase contrast research Wayanad Region with their prevalence microscope without supravital staining and intensity of infection. or after staining with neutral red. Permanent slides of adult Materials and methods parasites were prepared after fixing them in 5% formalin under slight cover Study area glass pressure and staining with The study was carried out in the acetocarmine, following the procedure Wayanad Region of the Western Ghats outlined by Cantwell (1981). (latitude 11° 27’ and 15° 58’ North and Specimens were measured using 75° 47’ and 70° 27’ East longitude). the Nikon NIS Elements Imaging Western Ghats is a treasure trove of software. All measurements are in biological diversity in India and is micrometers (µm), as range followed by considered one of the “hottest hotspots” mean in parentheses. Illustrations were of biodiversity because of its very rich made using the Nikon Y-IDT drawing fauna and flora and the highest level of tube attached to the Nikon ECLIPSE Ni-U endemism. microscope and the details were added Collection localities Birakuppa, free hand from observations made on Chandhanathodu, Chennalode,
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
Digenean parasites of the water skipper Euphlyctis cyanophlyctis 749
live specimens. Photographs were taken the institution or practice at which the with a Nikon Y-TV55 camera. study was conducted.
Ethical approval Results All applicable international, national, and/or institutional guidelines Five species of digenetic for the care and use of animals were trematodes, D. mehrai, T. ranarum, H. followed. All procedures performed in mehransis, G. glottoides and Ganeo the study involving animals were in tigrinum were found infecting the accordance with the ethical standards of duodenum of the frog E. cyanophlyctis.
Table 1. Digenean parasites with their prevalence and intensity of infection. Name of the parasite Prevalence of infection Intensity of infection Diplodiscus mehrai 12 out of 100 frogs (12%) 20 from 12 infected frogs (1.7) 275 from 8 infected frogs Tremiorchis ranarum 8 out of 100 frogs (8%) (34.4) Halipegus mehransis 2 out of 100 frogs (2%) 4 from 2 infected frogs (2) 139 from 31 infected frogs Ganeo glottoides 31 out of 100 frogs (31% (4.5) Ganeo tigrinum 8 out of 100 frogs (8%) 23 from 8 infected frogs (2.9)
Family Paramphistomidae Fischoeder, Philippines. Srivastava (1934a) recorded 1901 a new variety, D. amphichrus var. magnus Genus: Diplodiscus Diesing, 1836 from E. cyanophlyctis from UP and Pande 1. Diplodiscus mehrai Pande, 1937 (1937) added another species, D. mehrai, (Figure 1) from the same host in Kumaon Hills. The genus Diplodiscus of the Singh (1954) regarded D. amphichrus family Diplodiscidae Cohn, 1904 was var. magnus and D. mehrai as synonyms erected by Diesing (1836) and ascribed of D. amphichrus. Mukherjee (1966) D. Subclavatus (Pallas, 1760) as its type further synonymised D. japonicus species. So far 17 species have been (Yamaguti, 1936) with D. amphichrus. added to this genus from amphibians. Of Fischthal and Thomas (1968) raised the these six valid species have been variety magnus of Srivastava to species reported from Indian amphibians by rank and considered that D. amphichrus Srivastava (1934b) Pande (1937), of Agarwal and Singh, (1979) as synonym Bhalerao (1937), Kaw (1950), Pandey of magnus and so were D. amphichrus D. and Chakrabarti (1968), Pandey (1969a), japonicus and D. mehrai. Pandey and Mukherjee and Ghosh (1972), Dwivedi Chakrabarty, (1968) and Pandey (1969a) (1977), Singh (1977) and Shinad and described two new species, D. lalli and D. Prasadan (2017a). They are Diplodiscus chauhani from H. tigrina and E. amphichrus Tubangui, 1933, D. cyanophlyctis, respectively and Pandey amphichrus magnus Srivastava, 1934, D. and Jain (1974) upheld the validity of D. mehrai Pande, 1937, D. lali Pandey and mehrai. Nama and Khichi (1973) Chakrabarty, 1968, D. chauhani described a new sub species, D. Pandey,1969 and D. cyanophlycti Shinad amphichrus brevis from E. cynophlyctis and Prasadan, 2017. and disagreed to the synonymy of D. Tubangui (1933) described D. mehrai to D. amphichrus. Srivastava amphichrus from Rana sp. in the (1982) suggested that D. lali and D.
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
750 Keloth and Kandambeth
chauhani are synonyms of D. amphichrus. 2. Tremiorchis ranarum Mehra and Srivastava (1982) also considered that Negi, 1926 (Figure 2) the genus is represented by two distinct Mehra and Negi (1926a) species D.amphichrus and D.mehrai in proposed the genus Tremiorchis of the India. Recently a new species, D. family Brachycoeliidae Looss, 1899 with cyanophlycti was added by Shinad and T. ranarum from H. tigerinus as the type Prasadan (2017a). species. Ten species of this genus have Remarks. The species is been reported so far. They are T. characterized by conical, aspinose body ranarum Mehra and Negi, 1926, T. with a blunt anterior end and broadly mehrai Rai, 1962, T. vitelloconfluentum round posterior end. It has a sub (Sic) Rai, 1962, T. attenuates Karyakarte, terminal and slightly oval oral sucker 1973, T. tigrinanum Simha et al., 1974, T. without oral diverticula and a large varanum Verma, 1930, T. mathuraensis posterior sucker at the posterior end of Swarup and Jain, 1977, T. spinophlyctis body; it has a small central additional Karyokarte and Palladwar, 1977, T. sucker. Its mouth is sub terminal and jamshedpurensis Hussain, 1989, and T. intestinal caeca is wide, extend along the jaini Srivastava and Saxena, 1983. lateral margin of body up to the level of Pandey and Agarwal (1981), with due posterior sucker. It has a single testis at juistification, considered T. mehrai, T. the middle of body and a small cirrus sac vitelloconfluentum, T. tigrinarum, T. behind the intestinal bifurcation. Its eggs mathurensis and T. spiniphlyctis as are large, oval and operculate. synonyms of T. ranarum. Rajendran and Twelve out of 100 E. cyanophlictis Janardanan (1993) elucidated the life were infected with D. mehrai and the cycle of T. ranarum. prevalence of infection is 12%. Twenty D. Remarks. The species is mehrai were recovered from 12 frogs characterized by elongate – oval body and therefore, the intensity of infection is with spines on the surface, except at the 1.7 (Table 1). posterior third. It has a sub terminal and Collection localities: Pakkam, roughly spherical oral sucker and a Payyambally, Chundel, Birakuppa and ventral sucker at about one – third Panamaram, Wayanad District. distance from the anterior end of body. Mouth is sub terminal, pharynx is small and thick walled, oesophagus is long narrow and intestinal caeca terminates just behind the anterior margin of anterior testes. It has a round or transversely ovoid testes and a round ovary. Numerous small eggs are present. Eight out of 100 E. cyanophlictis were infected with T. ranarum so the prevalence of infection was 8%. Two hundred and seventy five T. ranarum were recovered from eight frogs and the intensity of infection was 34.4 (Table 1).
Few frogs infected with T. Figure 1. Diplodiscus mehrai (A1 and A2). ranarum exhibited multiple infections with adult trematodes. Collection localities: Chundel, Family: Brachycoelidae Johnston, Panamaram and Pulpally, Wayanad 1912 District. Genus Tremiorchis Mehra and Negi, 1926
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
Digenean parasites of the water skipper Euphlyctis cyanophlyctis 751
Gupta and Chopra (1986), H. ambalensis from the same host. Pandey (1975) synonymised H. udaipurensis and H. ambalensis with H. mehransis. Remarks. The species is characterized by smooth, spindle shaped body with slightly tapering anterior end and a blunt posterior end. Sub terminal, circular oral sucker and large, prominent, muscular ventral sucker. Its mouth is sub terminal and intestinal caeca extend
laterally up to hind end of body. Its Figure 2. Tremiorchis ranarum (B1 and B2). testes are oval, post-acetabular and obliquely side by side and cirrus sac is poorly developed. Genital pore is median, Family: Hemiuridae Luhe, 1901 ventral to pharynx and ovary is post Genus Halipegus Looss, 1899 testicular and intercaecal. Uterus with 3. Halipegus mehransis Srivastava, large number of closely packed 1933 (Figure 3) transverse coils occupy most of the The genus Halipegus was intercaecal field in the forebody. established by Looss, 1899 with H. Two out of 100 E. cyanophlictis ovocaudatus Vulpian, 1859. Altogether were infected with H. mehransis and the 22 species of this genus have been prevalence of infection is 2%. Four H. reported from different parts of the mehransis were recovered from two world. The nine species reported from frogs and the intensity of infection is 2 India are H. ovocaudatus (Vulpian, 1859) (Table 1). Looss, 1899, H. longispina Klein, 1905, H. Multiple infection was observed mehransis Srivastava, 1933, H. mehransis in one E. cyanophlictis with H. Mehransis, mehransis Srivastava, 1933, H. mehransis G. glottoides and D. mehrai. minutes Srivastava, 1933, H. spindalis Collection locality: Pakkam, Sruivastava, 1933, H. udaipurensis Gupta Wayanad District. and 1967, H. occidualis Stafford, 1905, and H. ambalensis Gupta and Chopra, 1936. Rankin (1944), while reviewing the genus, synonymised H. longispina and H. spindalis with H. ovocaudatus and H. mehransis, respectively. Srivastava (1933a) recorded a new variety of H. Mehransis, H. mehransis var. Minutum. Bhalerao (1936c) abolished the variety and considered it as a synonym of H. mehransis. Some more species were described under the genus Halipegus from India. Klein (1905) described H. longispina from Indian frog. Rankin Figure 3. Halipegus mehransis (C1 and C2). (1944) treated H. longispina as synonym of H. ovocaudatus, the type species of the genus. Later Rankin (1944) synonymised Family: Lecithodendriidae (Luhe, both species as that of H. Mehransis. 1901) Odhner, 1901 Gupta and Agrawal (1967) described H. Genus Ganeo Klein, 1905 udaipurensis from E. cyanophlyctis and
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
752 Keloth and Kandambeth
4. Ganeo glottoides Klein, 1905 (Figure coiled, filled with oval operculate eggs. 4) Urinary bladder is V-shaped and The genus Ganeo of the family vitellaria on the lateral margin up to the Lecithodendriidae (Luhe, 1901) Odhner, posterior one – fourth. Cirrus sac is 1901 was proposed by Klein (1905) with above ventral sucker. Its gonopore opens G. glottoides as its type from E. on the lateral margin just above the hexadactylus from Tamil Nadu. Since position of caecal bifurcation. then 17 species have been added to the Thirty one out of 100 E. genus. They are G. glottoides Klein, 1905, cyanophlictis were infected with G. G. glottoides glottoides Klein, 1905, G. glottoides and the prevalence of infection attenuates Srivastava, 1933, G. bufonis is 31%. One hundred and thirty nine G. Fotedar, 1959, G. gastricus Srivastava, glottoides were recovered from 31 frogs 1933, G. glottoidea madrasensis Mehra and the intensity of infection is 4.5 (Table and Negi, 1928, G. korkei Bhalerao, 1936, 1). G. kumaonensis Pande, 1937, G. Multiple infection was observed punjabensis Gupta, 1954, G. srinagarensis in few frogs with G. glottoides G. tigrinum, Kaw, 1950, G. tigrinum Mehra and Negi, D. mehrai, H. mehransis and T. Ranarum. 1928, G. gazipurensis Pandey and Collection localities: Makkimala, Chakraborty, 1968, G. ankholensis Peechangode, Kammana, Pakam, Hafeezullah and Dutta, 1985, G. Chundel, Panamaram, Chooralmala, vitellosinistrum Dwivedi and Chauhan, Bairakuppa, Kavummandam and 1971, G. kawi Dwivedi and Chauhan, Pulpally, Wayanad District. 1971, G. bahurai Ghosh and Chauhan, 1982, G. lucknowensis Gupta and Jahan, 1976. Fotedar (1959) while reviewing the genus synonymised G. kumaonensis with G. tigrinum. Mukherjee and Ghosh (1970) synonymised G. attenuates with G. tigrinum. G. kawi and G. gazipurensis were synonymised with G. bufonis by Rao (1974) and Gupta and Jahan (1976) respectively. Later Gupta (1977) considered G. bufonis as a synonym of G. tigrinum. Rao and Kameswari (1976) synonymised G. korkei and G. punjabensis with G. tigrinum. Remarks. The species has an Figure 4. Ganeo glottoides (D1 and D2). elongate oval body with bluntly pointed anterior end, and broadly round posterior end. Body is covered with small 5. Ganeo tigrinum Mehra and Negi, spines which are closely set at the pre- 1928 (Figure 5) acetabular zone and gradually decrease G. tigrinum was described from H. in number behind ventral sucker. It has a tigerinus by Mehra and Negi (1928) and small, circular, sub terminal oral sucker from Rana and Bufo species by other and a slightly larger equatorial ventral workers (Mukherjee and Ghosh 1970, sucker. Its mouth is sub terminal and 1972; Agarwal and Singh, 1977). It was pharynx is thick walled and globular. It also reported from two more hosts, H. has long narrow oesophagus and crassus and Fejervarya sp. by Diengdoh intestinal caeca. Its testes are obliquely (1989) and Tandon et al. (2001), placed one behind the other in front of respectively. Brinesh and Janardanan ventral sucker and round ovary is just (2012) described the life cycle of G. below the posterior testes. Uterus is tigrinum.
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
Digenean parasites of the water skipper Euphlyctis cyanophlyctis 753
Remarks. The species is Acknowledgements characterised by elongate-oval body with bluntly pointed anterior end and broadly The authors are grateful to the round posterior end. Body is covered Kerala State Council for Science, with small spines which are closely set at Technology and Environment (KSCSTE), the pre-acetabular zone and gradually Government of Kerala for providing decreased in number behind ventral financial assistance in the form of a sucker. Its oral sucker is small, circular, major research project (SRS/220/2015/ sub terminal, smaller than ventral KSCSTE) to carry out this study. The sucker. Mouth is sub terminal, pharynx is permission accorded by the Department thick walled, globular, and oesophagus is of Forest and Wildlife, Government of long, narrow and intestinal caeca reaches Kerala (Order No WL10-63909/2016) up to the upper margin of posterior one- for collecting frogs from the Wayanad fifth. Its obliquely placed Testes are forest region is also gratefully larger than ovary, slightly tandem and acknowledged. The authors are indebted located above the ventral sucker. to Prof. K. P. Janardanan for critically Anterior testis is smaller than posterior going through the manuscript. testis. Vitellaria are present on the lateral margin up to the posterior one-fourth. Cirrus sac is above ventral sucker and Conflict of interest gonopore opens on the lateral margin The authors declare that that just above the position of caecal there is no conflict of interest between bifurcation. them. Eight out of 100 E. cyanophlictis were infected with and the G. tigrinum References prevalence of infection is 8%. Twenty three G. tigrinum were recovered from Bhalerao, G. D. On the trematodes of the eight frogs and the intensity of infection digestive tract of a common Indian frog, Rana is 2.9 (Table 1). tigrina, with a description of Centrovitus Multiple infection was observed pentadelphi n.g., n.sp. Parasitology, v. 18, in a few frogs with G. tigrinum, G. p. 154-159, 1926. https://doi.org/10.1017/ glottoides and D. mehrai. S0031182000005102 Collection localities: Kammana, Bhalerao, G. D. Studies on the helminths of Pakam, Payyambally, Chundel and India. Trematoda I. Journal of Panamaram, Wayanad District. Helminthology, v. 14, no. 3, p. 163-180, 1936a. https://doi.org/10.1017/S0022149X 00003679 Bhalerao, G. D. Studies on the helminths of India. Trematoda II. Journal of Helminthology, v. 14, no. 4, p. 181-206, 1936b. https://doi.org/10.1017/S0022149X 00004089 Bhalerao, G. D. Studies on the helminths of India. Trematoda III. Journal of Helminthology, v. 14, no. 4, p. 207-228, 1936c. https://doi.org/10.1017/S0022149X 00004090 Bhalerao, G. D. Studies on the helminths of India. Trematoda IV. Journal of Helminthology, v. 15, no. 2, p. 97-124, 1937. Figure 5. Ganeo tigrinum (E1 and E2). https://doi.org/10.1017/S0022149X000307 53
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
754 Keloth and Kandambeth
Brinesh, R.; Janardanan, K. P. Studies on the Gupta, N. K.; Chopra, R. On digenetic life cycle of Ganeo tigrinus Mehra & Negi, trematodes of amphibians from India. Part I. 1928 (Digenea). Systematic Parasitology, v. Research Bulletin of the Panjab 82, no. 1, p. 13-19, 2012. University, v. 35, p. 1-6, 1986. Brinesh, R.; Janardanan, K. P. The life history Gupta, P. D. Fauna of Rajastan, India, Part 8. of Pleurogenoides malampuzhensis sp. nov. Trematoda. Records of the Zoological (Digenea: Pleurogenidae) from amphibious Survey of India, v. 62, p. 171-190, 1970. and aquatic hosts in Kerala, India. Journal of Gupta, P. D. Studies on the genus Ganeoi Helminthology, v. 88, p. 230-236, 2014. Klein, 1905 (Trematoda. Lecithodendridae). https://doi.org/10.1017/S0022149X130000 Records of the Zoological Survey of India, 84 v. 72, p. 281-290, 1977. Cantwell, G. E. Methods for invertebrates. In: Gupta, S. P.; Agarwal, V. Two trematode Clark, G (Ed.). Staining procedures. parasites of Rana cyanophlictis from Udaipur Baltimore: Williams and Wilkins, 1981. (Rajastan). Proceedings of the National p. 255-280. Academy of Sciences, India Section B: Chauhan, B. S. Studies on the trematode fauna Biological Sciences, v. 36, p. 530-536, 1966. of India. Part. IV. Subclass Digenea Gupta, S. P.; Agrawal, V. On a new trematode, (Prosostomata) (A revision of Hemiuroidea Halipegus udaipurensis n.sp. from Rana from Indian Region). Records of the Indian cyanophlyctis from Udaipur. Indian Journal Museum, v. 51, no. 2, p. 289-393, 1954. of Helminthology, v. 19, p. 77-80, 1967. Diengdoh, C. R. Helminth parasite Gupta, V.; Jahan, A. On two new trematode spectrum of amphibian hosts in parasites of amphibian from Lucknow. Meghalaya. Shillong: North-Eastern Hill Indian Journal of Helminthology, v. 28, p. University, 1989. (Thesis of doctorate). 141-147, 1976. Diesing, K. M. Monographie der Gattung Janardanan, K. P.; Prasadan, P. K. Studres on Amphistome und Diplodiscus. Annalen des the life-cycle of Pleurogenoides ovatus Rao, Wiener Museums der Naturgeschichte, 1977 (Trematoda: Pleurogenetinae). Journal v. 1, p. 235-260, 1836. of Helminthology, v. 65, no. 1, p. 43-50, Duda, P. L.; Verma, A. K. Role of gastropods in 1991. https://doi.org/10.1017/S0022149X trematode transmission among amphibians: 00010427 A numerical analysis. In: Koul, B. L. (Ed.). Janardanan, K. P.; Shanavas, K. R.; Usha, N. V. Advances in fish and wildlife ecology and On the progenetic metacercaia of biology. New Delhi 1: Daya Publishing Pleurogenordes ovatus Rao, 1977 House, 1996. p. 236-239. (Trematoda: Pleurogenetinae) from the Dwivedi, M. P. Incidence of trematodes in a freshwater crab, Paratelphusa hydrodromous particular species of frog population. Indian (Herbst), with observation on its in vitro Journal of Helminthology, v. 27, p. 25-32, excystment. Zoologischer Anzeiger, v. 219, 1977. p. 313-320, 1987. Fischthal, J. H.; Thomas, J. D. Digenetic Kaw, B. L. Studies in Helminthology. trematodes of amphibians and reptiles from Helminth parasites of Kashmir. Part I Ghana. Proceedings of the Trematoda. Indian Journal of Helminthological Society of Washington, Helminthology, v. 2, p. 67-126, 1950. v. 35, p. 1-15, 1968. Klein, W. Neue Distomen aus Rana Fotedar, D. N. On a new species of the genus hexadactyla. Zoologische Jahrbücher. Ganeo Klein, 1905 and some notes on the Abteilung für Systematik, Geographie und genus. Journal of Helminthology, v. 33, Biologie der Tiere, v. 22, p. 1-22, 1905. n. 2/3, p. 151-160, 1959. https://doi.org/ Looss, A. Weitere Beitrage zun Kenntniss der 10.1017/S0022149X00033393 Trematoden: Fauna Aegyptens. Zoologische Frost, D. R. Amphibian species of the world. Jahrbücher. Abteilung für Systematik, Version 6.0. Electronic Database, 2014. Geographie und Biologie der Tiere, v. 12, Available from:
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
Digenean parasites of the water skipper Euphlyctis cyanophlyctis 755
Parasitology, v. 18, no. 2, p. 168-181, 1926a. Pandey, K. C.; Chakrabarti, K. K. On a new https://doi.org/10.1017/S00311820000051 trematode Diplodiscus lali n.sp. from the 26 common Indian frog Rana tigrina Daud. Mehra, H. R.; Negi, P. S. The trematode Ceylon Journal of Science (Biological parasites of Rana tigrina of the Family Sciences), v. 8, p. 38-41, 1968. Pleurogenetinae Luhe. Proceedings of the Pandey, K. C.; Jain, K. M. Diplodiscus mehrai Indian Science Congress, v. 13, p. 185-186, Pande, 1937 from the common apple 1926b. snail Pila globusa Seainson, at Lucknow. Mehra, H. R.; Negi, P. S. Trematode parasites Journal of the Zoological Society of India, of the Pleurogenetinae from Rana tigrina v. 26, p. 145-147, 1974. with a revision and synopsis of the sub Rajendran, K. V.; Janardanan, K. P. Studies on family. Allah Univiversity Study, v. 4, p. 63- the life-cycle of Tremiorchis ranarum. 118, 1928. Journal of Helminthology, v. 67, no. 2, p. 95- Mukherjee, R. P. On some amphistomes of 101, 1993. https://doi.org/10.1017/S0022 India. Indian Journal of Helminthology, 149X00012955 v. 28, p. 94-103, 1966. Rankin, J. S. A review of the trematode genus Mukherjee, R. P.; Ghosh, R. K. Studies on some Halipegus Looss, 1899, with an account of the amphibian trematodes from Uttar Pradesh life history if H. ampherstensis n. sp. and West Bengal. (Part I). Indian Journal of Transactions of the American Helminthology, v. 22, p. 61-78, 1970. Microscopical Society, v. 63, p. 149-164, 1944. Mukherjee, R. P.; Ghosh, R. K. Studies on some amphibian trematodes from West Bengal and Rao, L. N. A note on the synonymy of Ganeo Maharashtra (Part II). Records of the kawi Dwivedi and Chauhan, 1970 with G. Zoological Survey of India, v. 66, p. 273- bufonis Fotedar, 1959. Current Science, 276, 1972. v. 43, p. 285-286, 1974. Nama, H. S.; Khichi, P. S. A new trematode and Rao, L. N.; Kameswari, M. On the synonymy of a new nematode from the frog Rana Ganeo korkei Bhalerao, 1936 and G. cyanophlictis Schneider. Proceedings of the punjabensis Gupta, 1954 with G. tigrinum Zoological Society, v. 26, p. 15-19, 1973. Mehra and Negi, 1928. Current Science, v. 45, p. 623-624, 1976. Pande, B. P. On some digenetic trematodes from Rana cyanophlyctis of Kumaon hills. Schneider, J. G. Historia Aphibiorum Proceedings of the Indian Academy of Naturalis et Literarariae. Fasciculus Sciences - Section B, v. 6, p. 109-120, 1937. Primus. Continens Ranas, Calamitas, Bufones, https://doi.org/10.1007/BF03051116 Salamandras et Hydros in Genera et Species Descriptos Notisque Suis Distinctos. Jena: Pandey, K. C. On a new trematode Diplodiscus Friederici Frommani, 1799. chauhani n. sp. from the common Indian frog, Rana cyanophlictis Schneider. Proceedings Shinad, K.; Prasadan, P. K. Description of of the Indian Academy of Sciences - Diplodiscus cyanophlycti n.sp. (Digenea: Section B, v. 29, p. 203-206, 1969a. Paramphistomidae) and prevalence and https://doi.org/10.1007/BF03051722 intensity of two other digeneans infecting the water skipper, Euphlyctis cyanophlyctis from Pandey, K. C. A redisription of Halipegus the Western Ghats, India. International mehransis Srivastava 1933 from the common Journal of Fisheries and Aquatic Studies, Indian frog, Rana cyanophlictis Schneider. v. 5, p. 259-263, 2017a. Available from: , v. 21, Indian Journal of Helminthology
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.
756 Keloth and Kandambeth
Shinad, K.; Prasadan, P. K. Two new species of Srivastava, H. D. On new trematodes of frogs Pleurogenoides (Luhe, 1901) Travassos, 1921 and fishes of the United Provinces, India. Part (Digenea: Pleurogenidae) infecting two II. Three new trematodes of the Subfamily species of frogs of the Western Ghats, India. Pleurogenetinae (Family Lecithodendriidae) Journal of Parasitic Diseases, v. 42, p. 130- from Rana cyanophlyctis of Oudh. Bulletin of 136, 2018a. https://doi.org/10.1007/ the Academy of Sciences of the United s12639-018-0978-y Provinces of Agra and Oudh, v. 3, p. 41-60, Shinad, K.; Prasadan, P. K. First record of 1933b. Encyclometra colubrimurorum (Rudolphi, Srivastava, H. D. On new trematodes of frogs 1819) Dollfus, 1929 (Digenea: and fishes of the United Provinces, India. Part Plagiorchiidae) metacercariae from a tadpole III. On a new genus Mehraorchis and two new and an adult frog of the Western Ghats, India. species of Pleurogenes (Pleurogenetinae) International Journal of Fisheries and with a systematic discussion and revision of Aquatic Studies, v. 6, p. 135-139, 2018b. the Family Lecithodendriidae. Bulletin of the Available from:
License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Braz. J. Biol. Sci., 2018, v. 5, No. 11, p. 747-756.