Protistology 6 (4), 290–296 (2010/11) Protistology

Myxodavisia haldarae sp. n. and sardinellae sp. n. (, ) from the gallbladder of Indian Sardine Sardinella longiceps collected in the Bay of Bengal

Nirmal Kumar Sarkar

Department of Zoology, Rishi Bankim Chandra College, Naihati, West Bengal, India

Summary

Two bivalvulid myxosporea Myxodavisia haldarae sp. n. and Ceratomyxa sardinellae sp. n. have been described from the gallbladder of Sardinella longiceps collected in the Bay of Bengal coast of West Bengal, India. The salient features of M. haldarae are: a large spore, backwardly directed shell valves end into sharp spine, spore- body 13.2 ± 1.42 (12-15) µm × 8.4 ± 0.74 (7.5-9) µm; polar capsule spherical 4.0 ± 0.71 (3-4.5) µm, and the characters of C. sardinellae – disporic sporogony, a small spore, broadly round ends of shell valves, suture distinct, 8.05 ± 1.095 (6.75-9) µm × 14.25 ± 1.061 (13.5-15.75) µm; polar capsule spherical 2.45 ± 0.35 (1.95-2.7) µm. These two species differ from the related species, which is demonstrated in the respective table.

Key words: Myxosporea, Bivalvulid, Ceratomyxa sardinellae sp. n., Myxodavisia haldarae sp. n, Sardine fish, The Bay of Bengal, West Bengal

Introduction The myxoporeans are either histozoic or coelo- zoic. About 2200 described species under 60 genera Myxozoans are usually the parasites of fish (both are known today (Fiala 2006).The present two freshwater and marine) but also found in amphibians species of the genera Ceratomyxa Thelohan 1892 and reptiles (Lom and Dykova, 2006). Recently and Myxodavisia Zhao et al. 2008 are coelozoic – a species Myxidiun anatidum from waterfowl inhabiting the gallbladder of a marine fish Sardinella (Bartholomew et al. 2008) and a species Soricimyx- longiceps the most studied myxosporea genera in um fegati from shrews (Prunescu et al. 2007) have this decade of the 21st century, because more than been reported from bird and mammal respectively. 25 new Ceratomyxa spp. have been described from The Phylum Grasse 1970 includes two marine fish of Australia (Gunter et al. 2008, 2009, classes – Myxosporea Butschli 1881 having all the 2010; Heiniger et al. 2008), South Africa (Reed et species reported from the vertebrate-invertebrate al.2007) and India ( Sarkar 2009, 2010). Moreover, hosts and Malacosporea Canning et al. 2000 having Adlard et al. 2010 proposed the demise of the the species reported from the Bryozoans. Leptotheca and transferred 47 Leptotheca

© 2011 by Russia, Protistology Protistology · 291 species to Ceratomyxa. The genus Myxodavisia is a of turn of polar filament in each capsule not discern- replacement name of Davisia as the later name was able; extra-capsular spore cavity with a dikaryotic or preoccupied by Davisia Del Guercio,1909 (Insecta: two monokaryotic sporoplasms; Measurements (N Hemiptera) and transferred 28 Davisia spp. to a new = 20 fresh spores): Spb - 13.2 ± 1.418 (12.0-15.0) genus Myxodavisia with the description of a new µm×8.4 ± 0.74 (7.5-9.0) µm; LApn - 32.5 ± 2.83 species M. sebastisca (Zhao et al. 2008). Recently (28.5-34.5) µm; Pcd -.4.0 ± 0.71 (3.0-4.5) µm. one more species has been added to the list (Sarkar 2010). The present paper describes a species of Taxonomic summary Myxodavisia Zhao et al. 2008 and a species of Host: Sardinella longiceps Valenciennes. Ceratomyxa Thelohan, 1892. Site of Infection: Gallbladder. Incidence: 1/35 (2.8%). Locality: The Bay of Bengal (Indian Ocean) Material and methods coast of West Bengal, India. Period of Infection: Early winter of 2009. The fishes were collected from Digha in Midna- Material: Syntypes material on the slide No. pur of the Bay of Bengal coast of West Bengal, India, Mxd – 17, deposited to the Parasitology Section of preserved with ice and brought to the laboratory the Zoological Survey of India, Kolkata. where autopsies were done from time to time under Remarks: The present species, among all known 10 × 45 magnification of a research microscope for Myxodavisia spp., overlaps with Myxodavisia spinusa the myxosporean parasite. The contact smears of (Davis, 1917) Zhao et al. 2008 in morphology of the infected tissue were made. The fresh wet smears spore but the length of the shell valve appendage of spores with a drop of Lugol’s iodine were studied of the former is about half the length of M. spinusa under 10 × 100 (oil immersion), measured (N = total (Table 1). The species in study is also relatively similar number of spore measured; mean ± SD; the range in shape of the spore to M. cyanoglossi (Laird, 1953) is provided in parenthesis), and photographed. The Zhao et al. 2008 and M. anoplopoma (Moser and dry smears were stained with Giemsa (1:15) after Noble,1975) Zhao et al. 2008, but their spore-bodies prefixation in absolute methanol. The descriptions are larger than the present species. The spore-bodies of species were made after Lom and Arthur (1989). of M. hexagrammi (Zhao et al.2002) Zhao et al. 2008, The figures were drawn with the help of Camera M. branchiophora (Davis,1917) Zhao et al. 2008, Lucida (Prism type) in combination with Corel M. ophidioni (Zaika, 1966) Zhao et al. 2008, M. Draw 12 version. The microphotographs were cornuta (Yurakhno and Naidenova, 2000) Zhao et taken by standard equipment from fresh and stained al. 2008, and M. cella (Jameson, 1931) Zhao et al. spores. The following abbreviations were used: Apn 2008 are smaller than the current species (Table 1). = Appendage, L = Length, Sp = Spore, Spb. = The spore-bodies of M. narvi (Aseeva, 2002), M. Spore-body, Std = Sutural diameter, Pcd = Polar reginae (Love et Moser, 1976) Zhao et al. 2008, M. capsule diameter, Pcdin = Polar capsule dimension, longifilus (Aseeva, 2003) Zhao et al. 2008, and M. SD = standard deviation and W = Width. sebastisca Zhao et al. 2008 although appear similar in dimensions, their appendages are very dissimilar in size and shape (Table 1). The current species has, Results therefore, been considered a new species for which the name Myxodavisia haldarae sp. n. is proposed. MYXODAVISIA HALDARAE SP. N. (FIGS. 1-3, 8, 9) Etymology:The species name is given to honor Prof. Dr. D. P. Haldar, an illustrious Protozoologist No early developmental or sporogonic stages of India. seen, mature spores laterally elongate triangular to ovoid spore-body and two long, sharp spine-like CERATOMYXA SARDINELLAE SP. N. (FIGS. 4-7, 10-13) lateral appendages, backwardly directed - one from each side of the respective shell valve of the spores; Plasmodium not observed but most likely suture distinct, vertical and slightly sinuous; shell polysporic and disporic: spores of typically cerato- valves smooth, laterally extended in the form of myxid type - almost hemispherical or subspherical, sharp spine-like appendages, rarely unequal, sepa- small with strongly arched anterior and straight rating membrane of respective appendage from the posterior surfaces; shell valves smooth with broadly spore body distinct (Figs 1-3); two equal, spherical round lateral ends and much thicker arched end to ovoid polar capsules slightly converging , number and thinner straight end in oblique view; suture 292 · Nirmal Kumar Sarkar

Figs 1-7. Line drawing (Camera Lucida aided) of two myxosporea (Bivalvulida). 1-3 - Line drawing of Myxodavisia haldarae sp. n.: 1 - a fresh spore in sutural view, Lugol’s iodine, 2 - a fresh spore with widely placed spines of shell valves, Lugol’s iodine, 3 - a fresh spore with converging spines, Lugol’s iodine; 4-7 - line drawing of Ceratomyxa sardinellae sp. n.: 4 - a fresh spore in sutural view, Lugol’s iodine, 5 - a fresh spore in top view, Lugol’s iodine, 6 - a Giemsa-stained spore with extruded polar filaments, 7 - a typical triradiate spore, Lugol’s iodine. vertical, slightly bent; two polar capsules spherical Taxonomic summary and equal, placed on the arched surface lying slightly Host: Sardinella longiceps Valenciennes. away from each other but seen at the centre in top Site of infection: Gallbladder. view; polar filament in the capsule not discernable Incidence: 1/35 (2.8). but when extruded reaching about 16.0-24.0 µm in Locality: The Bay of Bengal coast of West length; a binucleate, undifferentiated sporoplasm Bengal, India. observed in the extra-capsular spore cavity of the Material: Syntypes on the slide No. MxCr. spore. Triradiate spores with three spherical polar 12, deposited to the Parasitology Section of the capsules corresponding to three shell valves also Zoological Survey of India, Kolkata. seen; Measurements (N = 25 fresh spores, in µm): Remarks: About 170 species of the genus Spore – 8.05±1.096 (6.75-9.0)×14.25±1.061 (13.5- Ceratomyxa Thelohan,1892 are the most common 15.75); Polar capsule - 2.45±0.354 (1.95-2.7) in coelozoic myxosporea of marine fish (Eiras 2006, diameter. Reed et al. 2007, Heiniger et al. 2008, Sarkar 2009, Protistology · 293

Further, relatively similar other species of the genus Ceratomyxa (Table 2) differ by crescent or ovoid spores, larger or smaller dimension of spores, and different shape of the polar capsule, except for C. acanthopagri and C. adeli. In two latter species the polar capsules are spherical and resembles the ones of the present species. But the dimensions of spores of C. acanthopagri and C. adeli are dissimilar to the spore of the present Ceratomyxa sp. The species under study is also relatively similar in the shape of the spore to C. ernsti Gunter et al. 2010 and C. jonesi Gunter et al. 2010, but its dimensions do not comply with the later two species (Table 2). It is therefore imperative that the current species is a new species, for which the name Ceratomyxa sardinellae sp. n. is proposed. Etymology: The species name is given after the name of the host.

Acknowledgements

Author expresses sincere gratitude to P. K. Manna, the head of PG-Department of Zoology for Laboratory and Library facilities. He is also thankful Figs 8-13. Micrographs of two myxosporea (Bi- to Shyamal Das and Swapan Majhi, the fishermen, valvulida). 8, 9 - Myxodavisia haldarae sp. n., for collecting fish. 8 - a Giemsa-stained spore with the separated spore-body (arrow head), 9 - a Giemsa-stained spore showing the distinct spherical polar capsule; References 10-13 - Ceratomyxa sardinellae sp. n., 10 - a group of fresh spores, Lugol’s iodine, 11 - a pair of fresh Aseeva N.L. 2002. New species of myxosporea spores indicating disporic sporogony, Lugol’s (Myxozoa: Myxosporea) from sculpins of the iodine, 12 - a Giemsa-stained spore in sutural view, Northwestern Japan Sea. Acta Parasitol. 47, 13 - a Giemsa-stained spore with the extruded polar 179–189. filament from the polar capsule. Abbreviations: pc Aseeva N.L. 2003. New species of myxosporean – polar capsule, pf - polar filament, s - spore, st- (Myxozoa: Myxosporea) parasites of Ceratomyxa suture, sv – shell valve. Scale bars = 10 µm. from fishes of Peter Great Bay (Japan Sea). J. Parasitol. 89, 1172–1180. Gunter and Adlard 2008, 2009). Besides, recently Bakay Y.I.and Grudnev M.A. 1998. New 43 species of Leptotheca Thelohan 1895 have been species of Myxosporidia (Cnidospora: Myxosporea) assigned to Ceratomyxa Thelohan 1892 (Gunter in red fishes of the North Atlantic. Parazitol. 32, et al. 2010). The present Ceratomyxa sp. having 372–375(in Russian) small, subspherical spores resembles superficially Bartholomew J.L., Atkinson S.D., Hallett S.L., Ceratomyxa scissura (Davis 1917) Gunter et al. Lowenstine L.J., Garner M.M., Gardiner C.H., 2010, C. fisheri Jamason 1929, C. australis Gaevskya Rideout B.A., Keel M.K. and Brown J.D. 2008. and Kovaleva, 1979, C. cottoidii Reed et al. 2007, Myxozoan in waterfowl. Intl. J. Parasitol. C. honckenii Reed et al.2007, C. acanthopagri 38, 1199–1207. (Zhao and Song, 2003) Gunter et al. 2010, and Canning E.U., Curry A., Fiest S.W., Longshaw C. adeli (Bakay and Grudnev, 1998) Gunter et M. and Okamura B. 2000. A new class and order of al. 2010. However, C. scissura differs by unequal myxozoans to accommodate parasites of bryozoans shell valves and larger dimension of a spore, and C. with ultratructural observations on Tetracapsula fisheri - by larger width. C. australis also differs by bryosalmonae (PKX organism). J. Euk. Microbiol. smaller sutural diameter and ovoid polar capsule. 47, 456–468. 294 · Nirmal Kumar Sarkar

Table 1. Myxodavisia spp. from marine fi sh (measurement in μm).

Myxosporea (host) Tissue Spore-body Appendage length Polar capsule Locality

Myxodavisia haldarae sp. n. 13.2 (12.0-15.0) × Spherical GB 32.5 (28.5-34.5) Bay of Bengal, India (Sardinella longiceps) 8.0 (7.5-9.0) 4.0 (3.0-4.5)

M. cynoglossi (Laird, 1953) Zhao et 14.24 (12.6-16.8) × Ovoid GB 20.8-36.4 Bay of Bengal, India al., 2008 (Cynoglossus sp.) 12.6 (11.4-15.8) 3.2 × 3.4

M. anoplopoma (Moser and Spherical UB 12.75 (12-14) × 15.20 Central and South Noble, 1975) Zhao et al., 2008 34.7 (30-38) 4.95 (4-6) KT (13.0-17.0) California coast, USA (Anoplopoma fi mbria) 5-7 coils

M. spinosa (Davis, 1917) Zhao et al., Spherical North Carolina coast, UB 13.0 × 7.0 70.0 2008 (Paralichthys ambigutta) 4.0 USA

M. hexagrammi (Zhao et al., 2002) 9.9 (9.5-10.5) × 10.8 Spherical Yellow Sea and Bohai Zhao et al., 2008 UB 52.4 (44-59) (10.0-12.0) 3.8 (3.5-4) Bay, China (Hexagramos otakii)

M. ophidioni (Zaika, 1966) Zhao et Spherical UB 9.1-11.7 × 13.0 21-29 Black Sea, Sevastopol al., 2008 (Ophidion rochei) 3.9-5.2

M. branchiophora (Davis, 1917) Zhao Spherical North Carolina Coast, UB 9.0-11.0 × 9.0 18-22 et al., 2008 (Paralicnthys albigutta) 3.5 USA

M. cornuta (Yurakhno and Pyriform Naidenova, 2000) Zhao et al., 2008 UB 8.8–10.6 × 9.4–11.9 11.3–12.0 Azov Sea 3.0-3.3 × 2.0-2.5 (Neogobius fl uviatilis)

M. longifi lus (Aseeva, 2003) Zhao et Pyriform UB 10.5-13.5 × 11.7-13.0 20.0-23.0 Japan Sea al., 2008 (Hippoglossoides dubius) 3.0-4.5 × 2.5-3.0

M. narvi (Aseeva, 2002) Zhao et al., Spherical UB 10.0–11.5 × 11.5-14.4 20.0-27.0 Japan Sea 2008 (Myxocephalus brabdtii) 4.0-4.5

M. cella (Jameson, 1931) Zhao et al., Spherical UB 8.0-10.0 × 9.0-13.0 25.0-35.0 California Coast, USA 2008 (Porichthys notatus) –

M. reginae (Love and Moser, 12.8 (11.0-15.0) × Pyriform-Spherical 1976) Zhao et al. 2008 (Sebastes UB 40.5 (28-85) California Coast, USA 14.8(12-20) x11.5 3.5 (2.5-4.5) serranoides)

M. sebastisca Zhao et al., 2008 13.1(12.7-13.6) × Spherical UB 25.3-46.0 East China Sea (Sebastiscus marmoratus) 12.3(10.9-13.6) 5.3-6.0

Abbreviations: GB – Gallbladder, KT – Kidney tubule, UB – Urinary bladder.

Chakravarty M. 1943. Studies on Myxosporidia Australia’s Great Barrier Reef. Parasitol. 135, from the common food fishes of Bengal. Proc. Ind. 1165–1178. Acad. Sci. 18, 21–35. Gunter N.L.and Adlard R.D. 2009. Seven Davis H. S.1917. The myxosporidia of the new species of Ceratomyxa from the gallbladder of Beaufort region; a systematic and biological study. serranids from Great Barrier Reef, Australia. Syst. Bull. U S. Br. Frs. 35, 199–252. Parasitol. 73, 1–11. Eiras J. C. 2006. Synopsis of the species of Gunter N.L.and Adlard R.D. 2010. The de- Ceratomyxa Thelohan,1892 (Myxozoa: Myxo- mise of Leptotheca Thelohan,1895 (Myxozoa: sporea: Cerotomyxidae). Syst. Parasitol. 65, Myxosporea: ) and assignment of 49–71. its species to Ceratomyxa Thelohan 1892 (My- Fiala I. 2006. The phylogeny of Myxosporea xosporea: Ceratomixydae), Ellipsomyxa Koie, 2003 (Myxozoa) based on small subunit ribosomal RNA (Myxosporea: Ceratomyxidae), Butschli, gene analysis. Intl. J. Parasitol. 36, 1521–1534. 1882 and Sphaerospora Thelohan,1892 (Myxosporea: Gaevskaya A.A. and Kovaleva A. 1979. Two new Sphaerosporidae). Syst. Parasitol. 75, 81–104. species of myxosporidia Davisia donecae sp. n. and Gunter N.L, Whipps C.M. and Adlard R.D. Ceratomyxa australis sp. n. from the horse mackerel 2009. Ceratomyxa (Myxozoa: Bivalvulida): Robust of the Southeastern Atlantic. Biol. Mor. Vladivos. taxon or genus of convenience? Intl. J. Parasitol. 3, 80–83 (in Russian). 39, 1395–1405 Gunter N.L.and Adlard R.D. 2008. Bivalvulidan Gunter N.L.Burger M.A.A.and Adlard R.D. (Myxozoa: Myxosporea) parasites of Damselfishes 2010. Morphometric and molecular characteriza- with description of twelve novel species from tion of four new Ceratomyxa species (Myxosporea: Protistology · 295

Table 2. Ceratomyxa spp. from marine fi sh (measurements in μm)

Myxosporea (host) Plasmodium Spore Polar capsule Tissue Locality

Elongate subspherical, anterior margin arched, Ceratomyxa sardinellae sp. n. Polysporic, posterior straight, Sv. ends Spherical Bay of Bengal, GB (Sardinella longiceps) Disporic round 2.45 (1.9-2.75) India 6.87 (6.0-8.2) x 15.5 (13.5-16.5) Stubby with broadly round ends, anterior convex and C. scissura (Davis,1917) Gunter and Off North Carolina, Disporic posterior straight, Sv. Round 4.0 GB Adlard, 2010 (Dasyatis hastate) USA unequal 11.0 x 22.0

Ovoid,anterior convex C. fi sheri Jameson,1929 posterior straight, Sv. equal Large, round Disporic GB USA (Hydrolagus colliei) with round end – 5.1-7.1 x 9.3-13.3

Anterior margin convex, C. scatophagi Chakravarty,1943 Ovoid Disporic posterior concave GB India (Scatophagus argus) 3.1-2.5 4.2-7.2 x 16.0-26.0

Crescent-shaped, Sv. C. gibba Meglitsch, 1960 asymmetric Pyriform, unequal New Zealand, Disporic 2.8 x 2.3 and GB (Congiopodus leucopaecilis) 6.9 (5.6-8) x 17 (14.2- 2.3 x 2.0 Pacifi c 18.9)

Anterior convex and posterior margin slightly C. australis Gaevskaya and Kovaleva, Ovoid Disporic concave to straight, Sv. GB Namibia, Atlantic 1979 (Trachurus capensis) 2-2.6 x 1.3 rarely unequal 4.0-5.3 x 13.3-15.0 Slightly crescent-shaped, posterior margin slightly C. ernsti Gunter et al. 2009 Spherical Disporic concave, Sv. unequal, GB GBR, Queensland (Sillago ciliata) 1.66 x 1.58 5.67(4.67-6.84) x 11.94(9.47-14.79) Slightly crescent-shaped, posterior margin slightly C. jonesi Gunter et.al., 2009 Spherical Moreton Bay, Disporic concave, Sv. unequal GB (Pseulabrus guentheri ) 1.92 x 1.81 Queensland 5.1(4.1-6.08) x 12.99 (11.17-16.45)

Crescent-shaped C. bryanti Gunter and Adlard, 2008 Ovoid GBR, Heron, Disporic 5.31(4.48-6.87) x 1.69 (1.49-1.97) x GB (Abudefduf whitleyi) Island, Queensland 15.12(10.1 - 19.42) 1.66 (1.32-1.92)

Broadly elliptical to crescsnt with round ends, anterior C. cottoidii Reed et al., 2007 convex and almost straight Ovoid De Hoop, South Disporic 2.7 (2.3-3.0) x 2.4 GB (Clinus cottoides) posterior margin (2.0-3.0) Africa 7.0 (6.5-8.0) x 18.2(17.0- 22.0)

Slightly crescent C. honckenii Reed et al., 2007 Ovoid 3.1 (3.0-3.2) De Hoop, South Disporic 7.8 (7.5-8.0) x 19.0 (18.0- GB (Amblyrhynchotes honckenii) x 3.0 (3.0-3.1) Africa 21.0)

Elongate ovoid to sub- C. acanthopagri (Zhao and spherical, Sv. with rounded Spherical Song, 2003) Gunter et al., 2010 Disporic ends, sutural ridge raised GB Off China 1.9 (1.7-2.3) (Acanthopagrus schlegelii) 9.4 (8.7-10.0) x 17.9 (16.0-20.0).

Ovoid, anterior arched C. adeli (Bakay and Grudnev, 1998) posterior margin concave Spherical Gunter and Adlard, 2010 Disporic GB North Atlantic with round ends 4.0 (Sebastes marinus) 12.0-13.0 x 18.62-20.0

Abbreviations: GB – Gallbladder, Sv. – Shell valve, GBR –Great Barrier Reef.

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Address for correspondence: Nirmal Kumar Sarkar, 28 Mogaltuli,Chinsurah 712101, West Bengal, India; e-mail: [email protected]