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Protistology 7 (3), 178-188 (2012)
Protistology
Thelohanellus (Myxozoa: Myxosporea: Bivalvulida) infections in major carp fish from Punjab wetlands (India)
Ranjeet Singh and Harpreet Kaur
Department of Zoology and Environmental Sciences, Punjabi University, Patiala, India
Summary
A survey of freshwater fish parasites in Harike and Kanjali wetlands of Punjab (India) revealed two new and two already known myxosporean species of the genus Thelohanellus Kudo, 1933 parasitizing various fish organs, such as caudal fin, skin of snout, and gill lamellae. Spores ofthe first species, T. globulosa sp. nov. (11.67 x 7.9 ^m) are oval to spherical in valvular view, with blunt anterior ends and broad rounded posterior ends. A polar capsule, measuring 5.3 x 4.8 ^m, is rounded, balloon-like and located eccentrically inside the spore body cavity. Shell valves are very thick (stained dark blue with Heidenhain’s Iron-haematoxylin). Spores of the second species, T. kanjalensis sp. nov. (11.67 x 6.6 ^m) are elongated. Their anterior end is acuminated and exhibits a distinct pore. The posterior end is rounded, with lateral sides nearly parallel to each other. The pyriform to oblong polar capsule (7.5 x 3.3 ^m) occupies more than a half of the spore body cavity. The prominent neck leads to the fine duct opening. Shell valves stain dark-blue with Iron-haematoxylin in the middle part of the spore body cavity. Spores of the third species, T. boggoti Qadri, 1962 (10.1 x5.0 ^m) are egg-shaped to ovoid in valvular view, with bluntly pointed anterior ends and broad rounded posterior ends. The polar capsule (5.0 x 3.1 ^m) is flask-shaped, with the distinct neck, and is located anteriorly. Spores of the fourth species, T. caudatusPagarkar and Das, 1993 (15.0 x 7.0 ^m) are pyriform in valvular view, with tapering and pointed anterior ends and broad rounded posterior ends. Their polar capsule (6.3 x 4.6 ^m) is oval, with the blunt anterior end and rounded posterior end.
Key words: Bivalvulida, Myxozoa, Thelohanellus, gill lamellae, carp fish, plasmodia, polar capsule, Harike and Kanjali wetlands, India
Introduction
In Punjab (India), there are 12 natural, 10 man-made wetlands covering 15,500 Ha area, and only 3 main wetlands are included in Ramsar list of
International importance, i.e., Harike, Kanjali and Ropar wetlands. These wetlands have extremely rich biodiversity supporting a variety of plant and animal life. Harike wetland, the largest freshwater wetlands in northern India, occupies 4100 Ha and harbors 16
© 2012 The Author(s)
Protistology © 2012 Protozoological Society Affiliated with RAS
species of freshwater fish (Punjab State Council for Science and Technology Chandigarh, 2002). Kanjali wetland with an area of 185 Ha supports diversity of resident and migratory birds, and nurtures as many as 17 fish species. These fish are vulnerable to various parasitic infections, out of which Myxozoa is emerging as the major group. Myxozoa cause production loss and deaths, and some fish have to be discarded because they are unsightly and not considered fit for human consumption.
According to the latest review (Lom and Dyko-va, 2006), the phylum Myxozoa includes 4 malaco-sporean and 2,180 myxosporean species of 62 genera. However, three more genera (Soricimyxum, Gadimyxa, Thelohanelloid) with a type species S. fegati (Prunescu et al., 2007) from the liver of Sorex araneus, G. atlantica (Koie et al., 2007) from the urinary system of Gadus morhua, and T. bengalensis (Sarkar, 2009) from the gall bladder of Arius sagor have been described subsequently. In India, Myxozoa have been studied insufficiently, predominantly in two states, West Bengal and Andhra Pradesh.
In northern India, Gupta and Khera (1987, 1988a, 1988b, 1988c, 1988d, 1989a, 1989b, 1990, 1991) recorded 25 species belonging to genera Myxobolus, Henneguya, Myxidium, Thelohanellus and Unicauda infecting freshwater fish.
Recently, Kaur and Singh (2008, 2008-2009, 2009, 2010a, 2010b, 2010/2011, 2011a, 2011b, 2011c, 2011d, 2011e, 2011f, 2012a, 2012b) and Singh and Kaur (2012) have described 18 new species ofthe genus Myxobolus and one new species of the genus Triangula from freshwater fish in wetlands of Punjab. Furthermore, Kaur and Singh (2012a) also provided a synopsis of Indian myxobolids and revised the keys to the phylum Myxozoa.
There are very few species of the genus Thelo-hanellus reported all over the world. Lom and Dykova (1992) enlisted 39 species in this genus. Basu and Haldar (1999) described a new species of Thelohanellus from the gills of hybrid carps and published a checklist of Thelohanellus spp. parasitizing fish in India. Basu with co-authors (2006) provided a synopsis of 32 Indian species belonging to the genus Thelohanellus including one new species, T. disporomorphus, infecting Indian major carp, Cirrhina mrigala.
Genus Thelohanellus is characterized by pyriform or broadly ellipsoidal spores (valvular view), which look slimmer in sutural view. Spores always have smooth valves and single pyriform polar capsules, with a single coil of the polar filament, or subsphe-rical polar capsules with two coils. Sporoplasms are binucleate, mostly with a spherical polysaccharide
inclusion (Lom and Dykova, 2006). These parasites are histozoic and infect freshwater fish.
Two new species, T. globulosa sp. nov. and T. kanjalensis sp. nov., and two already known species, T. boggoti Qadri, 1962 and T. caudatus Pagakar and Das, 1993, collected from caudal fin, skin of snout, and gill lamellae of various species of carp fish have been discovered as a part of the study of fish parasitofauna of Harike and Kanjali wetlands. Spores have been identified following the keys of Kaur and Singh (2012a), and assigned to the genus Thelohnaellus. Description has been prepared in accordance with guidelines of Lom and Arhtur (1989).
Material and methods
Fish were collected in Harike and Kanjali wetlands. In the laboratory, plasmodia were removed, placed on microscopic slides, and examined in the light microscope under 100x oil objective (Magnus inclined Trinocular microscope MLX-Tr) for the presence of myxospores. Fresh spores were treated with 8% KOH solution to stimulate extrusion of polar filaments. For permanent preparations, air-dried smears were stained with Ziehl-Neelsen and Iron-haematoxylin. Drawings of stained material were made with the aid of camera lucida. Spores were measured with a calibrated ocular micrometer. All measurements are presented in ^m as range values followed by mean ± standard deviation (SD) in parentheses. The abbreviations used in the paper are as follows: LS, Length of spore; WS, Width of spore; LPC, Length of polar capsule; WPC, Width of polar capsule; NC, Number of coils of polar filaments; SD, Standard deviation
Results and discussion
Thelohanellus boggoti Qadri, 1962 (Figs 1—3)
Plasmodia. Minute, present around gill lamellae. Each plasmodium contains 7-8 spores.
Spores (Table 1, measurements based on 7-8 spores in frontal view). Spores were histozoic, measured 10.1 x 5.0 ^m, egg-shaped to ovoidal in valvular view, with bluntly pointed anterior ends and broad rounded posterior ends. Shell valves were 0.65 ^m thick, smooth and symmetrical. Parietal folds were absent. Polar capsules were flask-shaped with distinct neck, measured 5.0 x
3.1 ^m and occupied half of the spore body cavity. A polar filament looked thin, formed 5 coils, and was arranged perpendicular to the polar capsule axis. When extruded at the anterior tip, the polar
b
Fig. 1. Line drawing (Camera Lucida) of T. boggoi Qadri, 1962 spores. a — Spore stained with Ziehl-Neelsen (valvular view); b — spore stained with Iron-haematoxylin; the polar filament is extruded. Scale bar: 0.005 mm.
filament was thread-like, 45.4 ^m long. One capsulogenic nucleus was present beneath the polar capsule measuring 1.6 ^m in diameter. Sporoplasms were agranular, homogenous, moon-shaped, and occupied all extracapsular space behind the polar capsule. Sporoplasms contained two sporoplasmic nuclei, each 1.33 ^m in diameter. An iodinophilous vacuole measured 1.4 ^m in diameter.
Remarks. The present observations (LS/WS:
2.1) on T. boggoti Qadri, 1962 are in conformity with the original description (LS/WS: 1.7), except for some variations in sizes of the spore and polar capsule. Earlier, this parasite was recorded from gills of Labeo boggot. A new host, Catla catla, and a new locality, Harike wetland, are recorded for this parasite (Table 2).
Thelohanellus caudatus Pagarkar and Das, 1993 (Figs 4—6)
Plasmodia. Small, white, spherical to round, 0.50.8 mm in diameter; 2-4 plasmodia were observed
i---1
%
2a
\ i
• i
2b
i---------------------------------1
3
Figs 2, 3. Micrographs of T. boggoi Qadri, 1962 spores. 2a — Spore stained with Ziehl-Neelsen;
2b — spores stained with Iron-haematoxylin; the polar filament is extruded; 3 — fresh spore. Scale bars: 10 ^m.
per one caudal fin; each plasmodium contained 12-13 spores.
Spores (Table 3, measurements based on 7-9 spores in frontal view). Spores were histozoic, measured 15.0 x 7.0 ^m, pyriform in valvular view, with tapering and pointed anterior ends and broad rounded posterior ends. The sutural ridge was distinct and straight. Shell valves were 0.4 ^m thin, smooth and symmetrical. Parietal folds were absent. Polar capsules were oval, measured 6.3 x 4.6 ^m, with blunt anterior ends and rounded posterior ends. The polar filament formed 5-6 coils and was arranged
Fig. 4. Line drawing (Camera Lucida) of T. cauda-tus Pagarkar and Das, 1933. a — Spore stained with Ziehl-Neelsen (valvular view); b — spore in the side view. Scale bar: 0.005 mm.
Table 1. Measurements (|-im) of T. boggoti Qadri, 1962.
Character Range Mean value SD
LS 9.8-10.4 10.1 0.42
WS 4.5-5.5 5.0 0.70
LPC 4.8-5.2 5.0 0.28
WPC 2.9-3.3 3.1 0.28
Ratio: LS/WS 2.1
NC 5
Parietal Folds absent
obliquely to the polar capsule axis. Sporoplasms occupied all extracapsular space behind polar capsules, and contained three sporoplasmic nuclei measuring 0.4-0.6 ^m in diameter. An iodinophilous vacuole was 3.16 ^m in diameter.
Figs 5, 6. Micrographs of T. caudats Pagarkar and Das, 1933 spores. 5a, b — Spores stained with Ziehl-Neelsen; 6 — fresh spores. Scale bars: 10 ^m.
Remarks. The present observations (LS/WS:
2.1) on T. caudatus Pagarkar and Das, 1993 are in conformity with the original description (LS/WS: 1.5), except for some minor variations in the size of spors and polar capsules. Earlier, this parasite
Table 2. Comparison of the original description of T. boggoti Qadri, 1962 with the specimens from the new geographic isolate (measurements are in micrometer).
Species Host Site of infection Locality Spore Polar capsule
T. boggoti (present study) T. boggoti Qadri, 1962 Catla catla Labeo boggot gill lamellae gills Harike wetland, Punjab (India) Andhra Pradesh (India) 10.1x5.0 11.0-12.0x 6.0-7.5 5.0x3.1 5.5-7.0x 3.6-4.0
Table 3. Measurements (|-im) of T. caudatus Pagarkar and Das, 1993.
Character Range Mean value SD
LS 14.8-15.2 15.0 0.28
WS 6.8-7.2 7.0 0.28
LPC 6.0-6.6 6.3 0.42
WPC 2.9-3.3 3.1 0.28
Ratio: LS/WS 2.1
NC 5-6
Parietal Folds absent
was recorded from rays of caudal fin and anal fin. A new locality, Kanjali wetland, is recorded for this parasite (Table 4).
Thelohanellus globulosa sp. nov. (Figs 7—9)
Plasmodia. Small, white to pale yellow, round, 0.7-0.8 mm in diameter; 2-5 plasmodia were observed per one caudal fin; each plasmodium contained 7-8 spores.
Spores (Table 5, measurements based on 6-9 spores in frontal view). Spores were histozoic, measured 11.67 x 7.9 ^m, oval to spherical in valvular view with blunt anterior and broad rounded posterior ends. Shell valves were 0.6 ^m thick, smooth, symmetrical. Shell valves looked thick and stained dark blue with Heidenhain’s Iron-haematoxylin. Parietal folds were absent. Polar capsules were rounded, balloon-like, measured 5.3 x 4.8 ^m and positioned eccentrically inside the spore body cavity. Polar filament was ribbon-like, formed 4-5 coils, and was arranged perpendicular to the polar capsule axis. When extruded, the polar filament was thread-like, 49.5 ^m long. Sporo-plasms were scanty and not clearly seen.
Differential diagnosis. The studied species was compared to 13 representatives of the genus Thelohanellus infecting fish (Table 6). It differs from all of them by morphometric characters. The novel species possess oval to spherical body outline, like T.parastromataeiand T. seni. However, the narrow anterior end with 2-3 parietal folds at the anteriolateral region in T. parastromataei, spores with two polar capsules, and a short taillike process in T. seni, differentiate both of them
a
Fig. 7. Line drawing (Camera Lucida) of T. globulosa sp. nov. a, b — Spores stained with Ziehl-Neelsen (valvular view); c — spore stained with Iron-haematoxylin; the polar filament is extruded. Scale bar: 0.005 mm.
from the present species. Furthermore, eccentric polar capsules, scanty sporoplasms and thicker shell valves, especially at the anterior and posterior parts, stained dark blue with Heidenhain’s Iron-haematoxylin, differentiate the present species from T. parastromataei and T. seni.
In view of these differences, we assign a myxo-zoan parasite of Cirrhina reba from Harike wetland to a new species of the genus Thelohanellus.
Taxonomic summary of T. globulosa sp. nov.
Plasmodia: small, white to pale yellow, round, 0.7-0.8 mm in diameter.
Spores: spores measure 11.67 x 7.9 ^m, oval to spherical in valvular view with blunt anterior end and broad rounded posterior end. Polar capsules rounded balloon-like, measure 5.3 x 4.8 ^m, and position eccentrically inside the spore body cavity.
Table 4. Comparison of the original description of T. caudatus Pagarkar and Das, 1993 with the specimens from the new geographic isolate (measurements are in micrometer).
Species Host Site of infection Locality Spore Polar capsule
T. caudatus (present study) T. caudatus Pagarkar and Das, 1993 Labeo calbasu L. rohita caudal fin caudal fin; anal fin Kanjali wetland, Punjab (India) West Bengal (India) 15.0x7.0 13.0-14.0x 8.5-9.5 6.3x4.6 7.0-7.5x5.0-5.5
Table 5. Measurements (|-im) of T. globulosa sp. nov.
Thelohanellus kanjalensts sp. nov. (Figs 10—12)
Character Range Mean value SD
LS 11.07-12.27 11.67 0.8
WS 7.6-8.2 7.9 0.42
LPC 4.8-5.8 5.3 0.72
WPC 4.3-5.3 4.8 0.70
Ratio: LS/WS 1.4
NC 4-5
Parietal Folds absent
Type host: Cirrhina reba (Hamilton, 1822) vern. chunni, mori, kursa.
Type locality: Harike wetland, Punjab, India.
Type specimen: paratypes are spores stained by Ziehl-Neelsen and Iron-haematoxylin, deposited in the museum of Department of Zoology, Punjabi University, Patiala, India- Slide No. TF/ ZN/04.04.2010 and TF/IH/04.04.2010.
Site of infection: Caudal fin.
Prevalence of infection: 46% (7/15).
Pathogenicity: non-pathogenic.
Etymology: the specific epithet globulosa highlights the globular-like shape of the parasite.
Plasmodia. Small, white, round, 0.4-0.5 mm in diameter, located on the skin of snout; each plasmodium contained 7-9 spores.
Spores (Table 7, measurements based on 9-11 spores in frontal view). Spores were histozoic, measured 11.67 x 6.6 ^m, elongate to oval, with the acuminated anterior end exhibiting a distinct pore, and rounded posterior end with lateral sides nearly parallel to each other. Shell valves were 0.41 ^m thin, smooth and symmetrical. Parietal folds were absent. Shell valves stained dark-blue (with Iron-haematoxylin) in the middle part of the spore body. Polar capsules were pyriform to oblong oval in shape, measured 7.5 x 3.3 ^m and occupied more than half of the spore body cavity. The prominent neck led to the fine duct opening outside the spore. The polar filament was thick, ribbon-like, formed 4-6 coils, and was arranged perpendicular to the polar capsule axis. When extruded, the polar filament was
94.1 ^m long. A capsulogenic nucleus was present just beneath the polar capsule and measured 0.4-0.6^m in diameter. Sporoplasms were agranular,
Table 6. Thelohanellus globulosa sp. nov. and morphologically similar species (measurements are in micrometer).
Species Host Site of infection Locality Spore Polar capsule
T. globulosa sp. nov. (present study) Cirrhina reba caudal fin Harike wetland, Punjab (India) 11.67x7.9 5.3x4.8
T. niloticus Gurley, 1893 Labeo niloticus skin of head Nile (Egypt) 5.0x3.5 —
T. seni (Southwell et Prashad, 1918) Chakravarty et Basu, 1948 Catla catla branchiae West Bengal (India) 12.48-14.94 8.56
T. mrigalae Tripathi, 1952 C. mrigala skin on the head West Bengal (India) 10.8-12.0x6.3-7.2 5.4-7.2x3.6-5.0
T. nikolski Akhmerov, 1955 Cyprinus carpio haematopterus fin Amur basin (Russia) 19.0-20.0x12.0 7.0x5.0-6.0
T. potaili Lalitha Kumari, 19б9 L. potail fin Andhra Pradesh (India) 13.0x8.2 5.9x4.3
T. parastromataei Narasimhamurti et al., 1990 Parastromataeus niger gall bladder Orissa coast (India) 11.18x9.46 8.6x6.88
T. sanjibi Sarkar and Ghosh, 1990 Mystus gulio kidney West Bengal (India) 12.52x8.27 4.52x4.0
T. sudevi Sarkar and Ghosh, 1990 Amblypharyngo-don mola kidney West Bengal (India) 14.05x5.87 5.17x2.65
T. caudatus Pagarkar et Das, 1993 L. rohita between rays of caudal fin and anal fin West Bengal (India) 13.8x9.0 7.02x5.07
T. orissae Haldar et al., 1997 C. mrigala gills Orissa (India) 7.29x3.11 3.72x2.32
T. avijiti Basu et Haldar, 2003 L. rohita dorsal fin West Bengal (India) 14.0x9.7 6.0x4.0
T. habibpuri Acharya et Dutta, 2007 L. rohita pectoral fin West Bengal (India) 13.0-14.3 (13.9)x8.0-9.0 (8.5) 6.0-6.5 (6.0)x4.1-5.0 (4.9)
T. imphlaensis Hemananda et al., 2010/2011 L. rohita gills Imphal, Manipur (India) 20.4-22.1 (21.33)x8.5-10.2 (9.43) 10.2-11.05 (10.79)x3.4.0-4.25 (3.78)
0
8a
8b
)
V /
9
Figs 8, 9. Micrographs of T. globulosa sp. nov. spores. 8a — Spore stained with Ziehl-Neelsen;
8b — spores stained with Iron-haematoxylin; the polar filament is extruded; 9 — fresh spore. Scale bars: 10 ^m.
homogenous and occupied all extracapsular space behind polar capsules with sporoplasmic nuclei,
0.8-0.9 ^m in diameter. An iodinophilous vacuole was absent.
Differential diagnosis. The studied species was compared to 21 Thelohanellus spp. infecting fish (Table 8). It differs from all these species by morphometric characters. Spores of the novel species are elongate to oval, with acuminated anterior ends, similar to T. mrigalae, T. sanjibi and T. sudevi. However, oval shaped spores with a slight knob-like projection at the anterior end in T.
Table 7. Measurements (|-im) of T. kanjalensis sp. nov.
Character Range Mean value SD
LS 11.4-11.8 11.67 0.28
WS 6.4-6.8 6.6 0.28
LPC 7.4-7.6 7.5 0.14
WPC 3.1-3.5 3.3 0.28
Ratio: LS/WS 1.7
NC 4-6
Parietal Folds absent
mrigalae, oval to spherical spores in T. sanjibi and T. sudevi differentiate them from the new species. The polar capsule of the described species was pyriform to oblong oval, with the prominent neck leading to the fine duct, which opened outside at the anterior end of the spore. The polar capsule occupied more than a half of the spore body cavity. In contrary to this, in T. mrigalae the polar capsule is oval, in T. sanjibi - broadly ovoid to almost spherical, and in T. sudevi it is pyriform and occupies nearly half of the spore body cavity. Furthermore, this new species can be distinguished from congeners by shell valves darkly stained mediolaterally.
In view of these differences, we assign a myxo-zoan parasite of Catla catla from Kanjali wetland to a new species of the genus Thelohanellus.
Taxonomic summary of T. kanjalensis sp. nov.
Plasmodia: small, white, round, 0.4-0.5 mm in diameter.
Spores: spores measure 11.67 x 6.6 ^m, elongate to oval, with acuminated anterior end having a distinct pore, and rounded posterior end with lateral sides nearly parallel to each other. Shell valves stain dark-blue with Iron-haematoxylin in the middle part ofthe spore body. Polar capsules pyriform to oblong oval in shape measure 7.5 x 3.3 ^m and occupy more than a half of the spore body cavity.
Type host: Catla catla (Hamilton, 1822) vern. thail.
Type locality: Kanjali wetland, Punjab, India.
Type specimen: paratypes are spores stained by Ziehl-Neelsen and Iron-haematoxylin, deposited in the museum of Department of Zoology, Punjabi University, Patiala, India- Slide No. C/I/ZN 10.05.2009 and C/I/IH 10.05.2009.
Site of infection: skin of snout.
Prevalence of infection: 30% (3/10).
Pathogenicity: non-pathogenic
Etymology: the specific epithet kanjalensis highlights the name of the type locality.
Fig. 10. Line drawing (Camera Lucida) of T. kanjalensis sp. nov. a, — Spores stained with Ziehl-Neelsen (valvular view); b — spore stained with Iron-haematoxylin; the polar filament is extruded. Scale bar: 0.005 mm.
Acknowledgements
The authors express thanks to University Grants Commission (UGC) for the financial support.
References
Acharya S. and Dutta T. 2007. Thelohanellus habibpuri sp. n. (Myxozoa: Bivalvulida) from the tropical freshwater fish rohu, Labeo rohita (Hamilton-Buchann, 1882) in West Bengal, India: Light and electron microscope observations. Anim. Biol. 57, 3, 293-300.
Akhmerov A.K. 1955. Ways of the origin of myxosporidian species of the genus Thelohanellus Kudo from Amur wild carp. Dokl. Akad. Nauk SSSR. 105, 1129-1132.
Basu S. and Haldar D.P. 1999. Thelohanellus bifurcata n. sp. a new species of the genus Thelo-hanellus from hybrid carps and checklist of the species of the genus described from Indian fishes. Proc. Zool. Soc. Calcutta. 52, 1, 115-124.
0 11a
4 9 5' nb
0 12
Figs 11, 12. Micrographs of T. kanjalensis sp. nov. spores. 11a — Spore stained with Ziehl-Neelsen;
11b — spores stained with Iron-haematoxylin, with extruded polar filaments; 10 — fresh spores. Scale bars: 10 ^m.
Basu S. and Haldar D.P. 2003. Observations on two new thelohanelloid species (Myxozoa: Bivalvulida) from Indian major carps of West Bengal, India. J. Parasitol. Appl. Anim. Biol. 12, 1-2, 15-24.
Basu S., Modak B.K. and Haldar D.P. 2006. Synopsis of the Indian species of the genus Thelohanellus Kudo, 1933 along with description of Thelohanellus disporomorphus sp. n. J. Parasitol. Appl. Anim. Biol. 15, 1&2, 81-94.
Chakravarty M. and Basu M.S. 1948. Observations on some myxosporidians parasitic in fishes,
Table 8. Thelohanellus kanjalensis sp. nov. and morphologically similar species (measurements are in micrometer).
Species Host Site of infection Locality Spore Polar capsule
T. kanjalensis sp. nov. (present study) Catla catla skin of snout Kanjali wetland, Punjab (India) 11.67x6.6 7.5x3.3
T. niloticus Gurley, 1893 Labeo niloticus skin of head Nile (Egypt) 5.0x3.5 -
T. mrigalae Tripathi, 1952 Cirrhina mrigala skin on the head West Bengal (India) 10.8-12.0(11.4) 5.4-7.2x3.6-5.0
T. gangeticus Tripathi, 1952 Chela bacaila muscles West Bengal (India) 16.2-17.5x5.4 7.2x2.5
T. nikolski Akhmerov, 1955 Cyprinus carpio haematopterus fin Amur basin (Russia) 19.0-20.0x12.0 7.0x5.0-6.0
T. chrysopomati Lalitha Kumari, 1969 Barbus chrysopoma gill contents Andhra Pradesh (India) 12.4x5.4 6.5x2.7
T. potaili Lalitha Kumari, 1969 L. potail fin Andhra Pradesh (India) 13.0x8.2 5.9x4.3
T. coeli Sarkar et Mazumdar, 1983 Tachysurus tenuispinis gall bladder West Bengal (India) 12.75x7.12 7.13x3.2
T. wallagoi Sarkar, 1985 Wallago attu gall bladder West Bengal (India) 9.25x4.85 5.47x2.71
T. bengalensis Sarkar et Raychaudhury, 1986 Catla catla gall bladder West Bengal (India) 10.0-12.0 (10.95)x 5.5-7.5(6.59) 3.75-7.0 (5.42)x 3.0-4.5(3.47)
T. valeti Fomena et Bouix, 1987 Barbus jae, B. aspilus intestine, muscles Africa 11.0-13.0x4.0-5.0; 13.5-19.5x4.0-7.0 5.5-7.0x2.0-3.0; 6.0-9.0x2.0-3.5
T. sanjibi Sarkar et Ghosh, 1990 Mystus gulio kidney West Bengal (India) 12.0-13.0(12.52)x 8.0-8.5(8.27) 4.0-5.0(4.52)x 3.5-4.5(4.0)
T. sudevi Sarkar et Ghosh, 1990 Amblypharyn-godon mola kidney West Bengal (India) 13.0-15.0 (14.0)x 5.0-6.5(5.87) 4.75-6.0(5.17)x 2.0-3.0(2.65)
T. assambai Fomea et al., 1994 Labeo sp. - Africa 10.5x6.0 7.5x2.7
T. costeae Sakiti, 1997 L. senegalensis gill Benin (Africa) 8.5-10.5 ((9.4)x 5.0-6.5(5.6) 4.0-5.5(4.8)x 2.0-3.0(2.6)
T. ndjamenaensis Kostoingue et al., 1999 L. parvus gills Chad (Central Africa) 10.0-11.0 (10.0)x 7.0-8.0 (7.3) 4.0-5.0 (4.2)x (3.0-5.0(3.2)
T. bicornei Kabre et al., 2002 L. coubie intestine Burkina Faso (Africa) 13.0-14.0 (13.5)x 8.0-9.0(8.4) 6.5-8.0 (7.2)x 3.5-4.0(3.7)
T. endodermitus Mukhopadhyay et Haldar, 2004 L. rohita undersurface of scales West Bengal (India) 13.66x5.35 7.14x3.0
T. habibpuri Acharya et Dutta (2007) L. rohita pectoral fin West Bengal (India) 13.0-14.3(13.9)x 8.0-9.0(8.5) 6.0-6.5(6.0)x 4.1-5.0(4.9)
T. zahrahae Szekely et al., 2009 Barbonymus gonionotus gills Malaysia 23.8x9.0 9.9x6.3
T. imphlaensis Hemananda et al., 2010/2011 L. rohita gills Imphal, Manipur (India) 20.4-22.1 (21.33)x 8.5-10.2 (9.43) 10.2-11.05 (10.79)x 3.4.0 - 4.25 (3.78)
with an account of nuclear cycles in one of them. Proc. Zool. Soc. Bengal. 1, 23-33.
Fomena A. and Bouix G. 1987. Contribution a l’etude des Myxosporidies des poissons d’eau douce du Cameroun. III. Especes nouvelles du genre Henneguya Thelohan, 1892 et Thelohanelus Kudo, 1933. Rev. Zool. Afr. 101, 43-53.
Fomena A., Marqués A., Bouix G. and Njine T. 1994. Myxobolus bilongi sp. n., Thelohanellus assambai sp. n. et Thelohanellus sanagaensis sp. n., Myxosporidies parasites de Labeo sp. (Teleostei: Cyprinidae) dans le bassin de la Sanaga
au Cameroun (Afrique centrale). Annales de la Faculté des Sciences de l’Université de Yaoundé I. 3, 131-142.
Gupta S. and Khera S. 1987. On the genera Henneguya Thelohan, 1892 and Unicauda Davis, 1944. Res. Bull.(Sci.) Panj. Univ. 38, 153-163.
Gupta S. and Khera S. 1988a. Review of the genus Myxobolus Bütschli, 1882. Res. Bull. (Sci.) Panj. Univ. 39, I-II, 45-48.
Gupta S. and Khera S. 1988b. On a new myxo-zoan parasite (Myxozoa) Lomosporus indicus gen. sp. n. from fresh water fishes, Labeo calbasu (Ham.).
Acta Protozool. 27, 171-175.
Gupta S. and Khera S. 1988c. On a new species, Myxidium labeonis from freshwater fishes of Punjab, India. Arch. Protistenkd. 136, 393-396.
Gupta S. and Khera S. 1988d. On one new and one already known species of the genus Myxobolus from freshwater fishes of India. Res. Bull. (Sci.) Panj. Univ. 39, III-IV, 173-179.
Gupta S. and Khera S. 1989a. Observations on Myxobolus haldari sp. nov. (Myxozoa: Myxosporea) from freshwater fishes of North India. Res. Bull. (Sci.) Panj. Univ. 40, 281-291.
Gupta S. and Khera S. 1989b. Observations on Myxobolus punjabensis sp. nov. (Myxozoa: Myxobolidae), parasitic on gills and fins of Labeo dyocheilus. Riv. Parasitol. 50, 131—138.
Gupta S. and Khera S. 1990. On three species of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) from freshwater fishes of Northern India. Indian J. Parasitol. 14, 1—8.
Gupta S. and Khera S. 1991. On some species of the genus Myxobolus (Myxozoa: Myxosporea) from freshwater fishes of India. Indian J. Parasitol. 15, 35-47.
Gurley R.S. 1893. On the classification of the Myxospora group of protozoan parasites infesting fishes. Bull. US Fish. Comm. 11, 407-431.
Haldar D.P., Samal K.K. and Mukhopadhyay D. 1997. Studies in the protozoan parasites of fishes in Orissa: five new species of the genera Henneguya, Thelohanellus and Unicauda (Myxozoa: Bivalvulida). J. Beng. Nat. Hist. Soc. 16, 50—63.
Hemananda T., Mohilal N., Bandyopadhyay P.K. and Mitra A.K. 2010/2011. Thelohanellus imphalensis sp. nov. (Myxozoa) infecting gills of a major carp Labeo rohita Hamilton 1822 from Thoubal, Manipur, India. Protistology. 6, 280— 283.
Kabre G.B., Sakiti N.G., Marques A. and Sawadogo L. 2002. Thelohanellus bicornei sp. n., (Myxosporea, Bivalvulida) a gill parasite of Labeo coubie Ruppel, 1832 (Osteichthyes, Cyprinidae) from Burkina Faso, West Africa. Parasite. 9, 219—223.
Kaur H. and Singh R. 2008. Observations on one new species, of genus Myxobolus — M. naini and rediscription of M. magauddi recorded from freshwater fishes of Kanjali Wetland of Punjab, India. Proc. 20th Natl. Congr. Parasitol. NEHU Shillong, India. pp. 75—79.
Kaur H. and Singh R. 2008-2009. Incidence of Myxozoan parasites in fresh water fishes of Punjab Wetlands. J. Punj. Acad. Sci. 5—6, 88—91.
Kaur H. and Singh R. 2009. A new myxosporean species, Myxobolus eirasi sp. nov., a known species
M. venkateshi Seenappa, Manohar (1981) from the Indian major carp fish Cirrhina mrigala (Ham). Protistology. 6, 126—130.
Kaur H. and Singh R. 2010a. A new myxosporean species Myxobolus sclerii sp. nov. and one known species M. stomum Ali et al. (2003) from two Indian major carp fishes. J. Parasit. Dis. 34, 33-39.
Kaur H. and Singh R. 2010b. One new myxo-sporidian species, Myxobolus slendrii sp. nov., one known species, M. punjabensis Gupta, Khera (1989) infecting freshwater fishes in wetlands of Punjab, India. Parasitol. Res. 106, 1043—1047.
Kaur H. and Singh R. 2010/2011. Two new species of Myxobolus (Myxosporea, Bivalvulida) from the Indian major carp Labeo rohita Hamilton, 1822. Protistology. 6, 264—270.
Kaur H. and Singh R. 2011a. Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) from freshwater fishes of Punjab Wetlands (India). J. Parasit. Dis. 35, 33—41.
Kaur H. and Singh R. 2011b. Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting an Indian major carp in Ropar and Kanjali wetlands (Punjab). J. Parasit. Dis. 35, 23—32.
Kaur H. and Singh R. 2011c. Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting an Indian major carp and a cat fish in wetlands of Punjab, India. J. Parasit. Dis. 35, 169-176.
Kaur H. and Singh R. 2011d. Two new species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting Indian freshwater fishes in Punjab Wetlands (India). Parasitol. Res. 108, 1075—1082.
Kaur H. and Singh R. 2011e. Myxobolus hari-kensis sp. nov. (Myxozoa: Myxobolidae) infecting fins of Cirrhina mrigala (Ham.) — an Indian major carp in Harike Wetland, Punjab (India). Parasitol. Res. 109, 6, 1699-1705.
Kaur H. and Singh R. 2011f. Two new and one already known species of Myxobolus (Myxozoa: Myxosporea: Bivalvulida) infecting gill lamellae of Indian major carp fishes in Ropar and Harike wetlands (Punjab). Proc. 22nd Natl. Congr. Parasitol. Univ. Kalyani, West Bengal, India. pp. 81—90.
Kaur H. and Singh R. 2012a. A synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Bivalvulida) parasitizing Indian fishes and a revised dichotomous key to myxosporean genera. Syst. Parasitol. 81, 17—37.
Kaur H. and Singh R. 2012b. One new myxosporean species, Triangula cirrhini sp. nov., and one known species, T. ludhianae (Syn. M. ludhianae Gupta and Khera, 1991) comb. n. (Myxozoa: Myxo-
sporea), infecting Indian major carp in Harike wetland of Punjab. Anim. Bio. 62, 129—139.
Koie M., Karlsbakk E. and Nylund A. 2007. A new genus Gadimyxa with three new species (Myxozoa, Parvicapsulidae) parasitic in marine fish (Gadidae) and the two-host life cycle of Gadimyxa atlantica n. sp. J. Parasitol. 93, 459—1467.
Kostoingue B., Fall M., Faye N. and Toguebaye B.S. 1999. Three new myxosporidian (Myxozoa: Myxosporea) parasites of freshwater fishes from Chad (Central Africa). Acta Protozool. 38, 323326.
Kudo R. 1933. A taxonomic consideration of Myxosporidia. Trans. Am. Microsc. Soc. 52, 195-216.
Lalitha Kumari P.S. 1969. Studies on parasitic protozoa (Myxosporidia) of fresh water fishes of Andhra Pradesh, India. Riv. Parasitol. 30, 153— 226.
Lom J. and Arthur J.R. 1989. A guideline for the preparation of species descriptions in Myxosporea. J. Fish Dis. 12, 151-156.
Lom J. and Dykova I. 1992. Myxosporidia (Phylum Myxozoa). In: Protozoan parasites of fishes. Developments in aquaculture and fisheries. (Eds. Lom J. and Dykova I.). Elsevier, Amsterdam. pp. 159-235.
Lom J. and Dykova I. 2006. Myxozoan genera: Definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 53, 1-36.
Mukhopadhyay D. and Haldar D.P. 2004. Thelohanellus endodermitus sp. n. A new Myxozoan (Myxozoa: Bivalvulida) from the major carp, Labeo rohita (Hamilton-Buchanon) in a sewage farm in West Bengal, India. Environ. Ecol. 22, 139—142.
Narasimhamurti C.C., Kalavati C., Anuradha
I. and Padma Dorothy K. 1990. Studies on the protozoan parasites of deep water fish from the Bay of Begal. Proc. Ist Workshop on Scientific Results of FORV Sagar Sampada. pp. 325—336.
Pagarkar A.U. and Das M. 1993. Two new species of myxozoa, Thelohanellus caudatus n. sp. and Myxobolus serrata n. sp. from cultural carps. J. Inland Fish Soc. India. 25, 30—35.
Prunescu C.C., Prunescu P., Pucek Z. and Lom J. 2007. The first finding ofmyxosporean development from plasmodia to spores in terrestrial mammals:
Soricimyxum fegati gen. et sp. n. (Myxozoa) from Sorex araneus (Soricomorpha). Folia Parasitol. 54, 159-164.
Qadri S.S. 1962. A new Myxosporidian Thelohanellus boggoti n. sp. from an Indian fresh water fish Labeo boggot. Arch. Protistenkd. 106, 218—222.
Sakiti G.N. 1997. Myxosporidies et Myxospo-ridies des poisons du Benin: faunistique, ultrastructure, biologie. These de doctorat d’E'tat, Universite ational du Benin. pp. 1—296.
Sarkar N.K. 1985. Some coelozoic Myxosporida (Myxozoa: Myxosporea) from a freshwater teleost fish of River Padma. Acta Protozool. 24, 1, 47—53.
Sarkar N.K. 2009. Thelohanelloid bengalensis gen. and sp. nov. (Myxosporea: Thelohanellidae) from the gall bladder of marine catfish of the Bay of Bengal, India. U. P. J. Zool. 29, 251-254.
Sarkar N.K. and Ghosh S. 1990. Two new myxozoan parasite ofthe genus Thelohanellus Kudo, 1933 (Myxosporea: Myxobolidae) from freshwater fishes of West Bengal, India. New Agricultrist. 1, 35-38.
Sarkar N.K. and Mazumdar S. 1983. Studies on myxosporidian parasites (Myxozoa: Myxosoma-tidae) from marine fishes in West Bengal, India. I. Description of three new species from Tachysurus sp. Arch. Protistenkd. 127, 59—63.
Sarkar N.K. and Raychaudhuri S. 1986. Thelohanellus bengalensis sp. n. and Myxidium mystuium sp. n. (Myxozoa): two new Myxosporidia from Indian freshwater teleost. Acta Protozool. 25, 3, 359-362.
Singh R. and Kaur H. 2012. Biodiversity of Myxozoan parasites infecting freshwater fishes of three main Wetlands of Punjab, India. Protistology. (in press).
Southwell T. and Prashad B. 1918. On some Myxosporidia. Parasites of Indian fishes with a note on the carcinoma in the climbing perch. II. Rec. Indian Mus. 15, 341—355.
Szekely C., Shaharom-Harrison F., Cech G., Mohamed K. and Molnar K. 2009. Myxozoan pathogens of Malaysian fishes cultured in ponds and net-cages. Dis. Aquat. Org. 83, 49—57.
Tripathi Y.R. 1952. Studies on the parasites of Indian fishes. I. Protozoa. Myxosporidia together with a Checklist ofparasitic protozoa described from Indian fishes. Rec. Indian Mus. 50, 63—88.
Address for correspondence: Ranjeet Singh, Harpreet Kaur. Department of Zoology and Environmental Sciences, Punjabi University, Patiala-147002, India; e-mail: ranjitsrana@gmail.com; harpreet_bimbm@yahoo.com
