Biodiversity of myxozoan parasites infecting freshwater fishes of three main wetlands of Punjab, India Текст научной статьи по специальности «Биологические науки»

Protistology 7 (2), 79-89 (2012)

Protistology

Biodiversity of myxozoan parasites infecting freshwater fishes of three main wetlands of Punjab, India

Ranjeet Singh and Harpreet Kaur

Department of Zoology and Environmental Sciences, Punjabi University, Patiala, India

Summary

Material pertaining to the present investigation was collected from three main wetlands of Punjab (included in Ramsar list oflnternational importance), i.e. Harike, Kanjali and Ropar wetlands. Extensive collection tours were made to these wetlands during the period from May, 2006 to April, 2010. A large number of important commercial fishes of these wetlands are vulnerable to various infections, out of which myxozoans are emerging as the major group. Various organs such as gills, fins, scales, skin, eye, stomach, intestine etc. were found to be infected with plasmodia of as many as 45 species of myxozoans representing 4 genera, namely, Myxobolus (26 species), Thelohanellus (16 species), Neothelohanellus (1 species) and Triangula (2 species) were recorded. Two species belonging to the genus Myxobolus, i.e. M. moli Fomena and co-authors (1985) and M. stomum Ali and co-authors (2003) were recorded from gills and scales of Amblypharyngodon mola and Labeo rohita respectively for the first time in India.

Key words: freshwater fishes, Myxozoa, Plasmodium, wetlands of Punjab

Introduction

Myxozoans are one of the economically important groups of microscopic metazoan parasites as they infect fish harvested for food. New myxosporean pathogens are continually emerging and threatening the development of pisciculture all over the world. They cause production losses and some fish have to be discarded because they are unsightly and not considered to be fit for human consumption. Myxozoans undergo a complex, multicellular development, culminating in the formation of a multicellular spore that is resistant to the external

environment. Markiw and Wolf (1983) and Wolf and Markiw (1984) made a landmark discovery on the life cycle of Myxobolus cerebralis involving alteration with an actinosporean form in Tubifex tubifex. Subsequently, involvement of annelid worms in the life cycle of some 30 other freshwater myxozoan have been documented (El-Matbouli and Hoffman, 1989, 1993; Kent et al., 1993a, 1993b; El-Mansy and Molnar, 1997; Eszterbauer et al., 2000; Kallert et al., 2005). Similar life cycle has also been described for other genera which include Henneguya, Sphaerospora, Ceratomyxa, Myxidium, Zschokkela, Thelohanellus, Hoferellus

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Protistology © 2012 Protozoological Society Affiliated with RAS

and Tetracapsula. New aquaculture practice such as intensive and polyculture systems have been widely introduced. Growing more fish on a limited area often resulted in increased disease outbreaks (Hoffman and Bauer, 1971).

Although myxozoans are best known for the infection they cause in teleost (bony fish), a small number of species have also been found parasitizing bryozoans, platyhelminths, annelids, marine fishes, amphibians, reptiles and birds. So far 19 species have been described from amphibians and reptiles belonging to the genera Myxobolus, Myxidium, Hoferellus, Chloromyxum, Caudomyxum and Spha-erospora (Eiras, 2005). Developmental stages were also found in waterfowl, in nervous system of mammals and were even detected in human faeces (Moncada et al., 2001) but no myxozoan has been known to be hazardous to human health.

Probably the most frequently cited example of myxozoan parasitism is the whirling disease, caused by M. cerebralis (Hedrick et al., 1998). In this case, the parasite infects the cartilages of the host’s head and spine, causing deformities that result in the characteristic whirling behavior. Others that are associated with host mortalities are Tetracapsuloides bryosalmonae, the cause of proliferative kidney disease in Pacific salmon (Kent et al., 2001), Enteromyxon leei, an intestinal parasite of Mediterranean sea bream (Diamant, 1992) and Henneguya ictaluri in pond-reared catfish (Pote et al., 2000). Recently, Hemananda and co-authors (2008) reported Henneguya manipurensis as the main cause of ulcerative disease syndrome in freshwater fish Anabas testudinus of Manipur (India).

These are just a few examples of myxozoans that play a role in causing diseases of commercially important fish. Most species of Kudoa are recognized for their impacts on marketability of commercially important fish host, rather than causing host mortalities. Egusa (1986) and Moran and co-authors (1999) observed that Kudoa thyrsites not only form muscle cysts, but are also responsible for post-mortem degradation in their hosts. Similar observations were also made by Kudo and coauthors (1987) and Yokoyama and co-authors (2004) that some species of Kudoa dwell in the myofiber by forming pseudocysts and cause postmortem myoliquification known as post harvest of flesh or jelly meat. Szczepaniak and co-authors (2010) discussed that cutaneous myxosporidiasis is common in fishes and is usually caused by species belonging to genera Myxobolus (M. squamae, M. ellipsoids, M. sandrae and M. cotlani), Sphaerospora (S. carassiiand S. molnari), Thelohanellus (T. dogieli) and Henneguya (H. wolinensis).

Dykova and co-authors (1986), Bauer and co-authors (1991) and Kovac-Geyer and Molnar (1983) observed that in farmed carp, Myxobolus spp caused locomotory disturbances coupled with emaciation and sunken eyes in the cases of brain infection, anaemia, haemorrhagic dropsy and mortality in the cases ofheavy cardiac infection and circulatory dysfunction in infection at the base of the gill lamellae respectively. Martins and co-authors (1997, 1999b), Adriano and co-authors (2005a, 2005b) and Feist and Longshaw (2006) recorded significant tissue damage and occasionally death in gill infections by myxosporea. Earlier, Rukyani

(1990) reported congestion caused by hypertrophy and inflammation due to rupture of cysts in cases of heavy infections with M. koiin gills of carp. Damage to the gills resulted in respiratory problems and fish were swimming near the surface with distended opercula. Dykova and Lom (1982) demonstrated that Sphaerospora renicola proliferating in the renal tubules damaged the renal tubuli epithelium and the released spores congested excretory passages in carp and gold fish. Paperna and Overstreet (1981) and Kalavati and Narashimhamurti (1985) reported that rupture of cysts that caused intense haemorrhage sometimes resulting in considerable loss of blood and facilitated invasion of secondary opportunistic pathogens.

In Punjab, there are 12 natural, 10 man-made wetlands covering the area of 15,500 ha. and only

3 main wetlands are included in Ramsar list of International importance, i.e. Harike, Kanjali and Ropar wetlands (Fig. 1). State has 2 other wetlands of national importance and 5 of state importance (ENVIS Centre, PSCST, Punjab; The Tribune, Feb 04, 2008). These wetlands have extremely rich biodiversity as they support a variety of plant and animal life. Out of 3 wetlands, the Harike wetland is located at the confluence of two major rivers of Punjab namely Sutlej and Beas. It falls in three districts ofAmritsar, Ferozepur and Kapurthala and is the largest freshwater wetland in northern India occupying 4,100 ha. It is ecologically important having an extremely rich biodiversity with as many as 26 species of fishes. Kanjali wetland with an area of 183 ha. supports diversity of resident and migratory birds, nurture large number of fish fauna with as many as 17 species of fishes. Ropar wetland is a unique wetland being located in the lap of Shivalik foothills, is an important habitat of many species and has tremendous ecological value, spread over 1,365 ha.; this wetland supports as many as 35 species of fishes. A large variety of fishes in these wetlands are vulnerable to various parasitic infections, out of which Myxozoa is emerging as the major group.

Fig. 1. Location map of wetlands in Punjab.

Material and methods

Fishes collected from Harike, Kanjali and Ropar wetlands were brought to the laboratory and examined for the myxozoan infection. Plasmodia when found were removed and teased on slide and covered with cover slip to examine the myxospores. Fresh spores were treated with 8% KOH solution for the extrusion of polar filaments. For permanent preparation, air-dried smears were stained with Ziehl-Neelsen and Iron-haematoxylin. Spores were measured with the help of a calibrated ocular micrometer. All measurements are in microns (^m). For calculations of prevalence, mean intensity and abundance, the following formulae were applied.

(a) Prevalence (%) =

Number of infected fish x 100 Total number of fish examined

Number of collected parasites

(b) Mean Intensity = Number of infected fish---------

(c) Abundance = Number of c°Hected parades

Number of fish examined

Results and discussion

During the present study on three wetlands of Punjab, a total of 1,397 fishes belonging to 7 families and 15 genera were examined for the presence of myxozoan parasites (Table 1). Different

organs such as gills, fins, scale, skin, eye ball and duodenum were found infected in 780 fishes with the 55.8% of infection. As many as 45 species of myxozoans representing 4 genera, namely, Myxobolus (26 species), Thelohanellus (16 species), Neothelohanellus (1 species) and Triangula (2 species) were recorded.

Prevalence rate was found to be the highest in Labeo rohita (72.7%) and L. bata (72.7%) followed by Labeo dero (33.3%) in Ropar wetland. In Kanjali wetland, the prevalence rate was highest in C. mrigala (85.4%) followed by Labeo calbasu (83.3%) and Labeo rohita (75%). In Harike wetland, the prevalence rate was highest in Wallago attu (84.6%) followed by Catla catla (83.3%) and Amblypharyngodon mola (66.6%) (Tables 2, 3 and 4). Fishes of Kanjali wetland were found to be more infected (71.1%) in comparison to Harike wetland (60.8%) followed by Ropar wetland (28.7%).

Two species belonging to the genus Myxobolus, i.e. M. moli (Fomena et al., 1985) and M. stomum (Ali et al., 2003) were recorded from gills and scales ofA. mola and L. rohita respectively for the first time in India.

In the three wetlands of Punjab, 13 species of carps, 2 species of catfishes (Wallago attu, Mystus seenghala), 2 species of murrels (Ophiocephalus punctatus, O. marulius) and 1 species each ofgourami (Colisa lalia), batchwas (Eutropiichthys murius)

S. No. Host examined Number examined Number infected Myxozoan parasites recorded

i Amblypharyngodon mola vern. mola carplet, molelia (common name: makhani) 30 10 Myxobolus moli Fomena et al., 1985 (revised diagnosis and new nomenclature Myxobolus sp. 4 Fomena et al.,1985)

2 Carassius carassius vern. crucian carp (common name: carp) 80 Nil -

З Catla catla vern. thail (common name: thail) 172 71 Myxoblus catli Kaur and Singh (2011c); M. magauddi (Bajpai et al., 1981) Gupta and Khera, 1988; M. parsi Das (1996); M. sclerii Kaur and Singh (2010a); Thelohanellus boggoti Qadri (1962); T. kanjalensis sp. nov. Singh (2011); T. mrigalae Tripathi (1952); T. mucousalis sp. nov. Singh (2011); T. thaili sp. nov. Singh (2011)

4 Cirrhina reba vern. mori, kursa (common name: mori, sunni) 50 35 Myxobolus kalmani Kaur and Singh (2011c); Triangula ludhianae (syn. Myxobolus ludhianae Gupta and Khera, 1991) Kaur and Singh, 2012; Thelohanellus kalavatae sp. nov. Singh (2011); T. haldari Singh (2011); T. globulosa Singh (2011); Triangula cirrhini Kaur and Singh (2012)

Б Cirrhina mrigala vern. mrigal (common name: naraini, marakh) 364 185 Myxobolus bhadurius (Sarkar 1985) Gupta and Khera, 1988; M. eirasi Kaur and Singh (2009); M. kanjali Kaur and Singh (2011d); M. mehl-horni Kaur and Singh (2011b); M.. naini Kaur and Singh (2008); M. punjabensis Gupta and Khera (1989); M. ropari Kaur and Singh (2011d); M. slendrii Kaur and Singh (20l0b); M. venkateshi Seenappa and Manohar (1981); M. harikensis Kaur and Singh (2011e)

б Colisa lalia vern. gurami (common name: dwarf gurami ) 20 Nil -

7 Ctenopharngodon idella vern. grass carp (common name: grass carp) 70 Nil -

а Cyprinus carpio vern. mirror carp (common name: mirror carp) 30 Nil -

9 Eutropiichthys murius vern. dhungi, piassi (common name: not known) 70 Nil -

io Hypophthalmichthys molitrix vern. silver carp, brigade (common name: silver carp) 30 Nil -

ii Labeo bata vern. bata (common name: bata) 37 8 Thelohanellus avijiti Basu and Haldar (2003)

i2 Labeo calbasu vern. kalbans (common name: kalbasu) 60 25 Myxobolus filamentosus (Haldar et al., 1981) Gupta and Khera, 1988; Thelohanellus caudatus Pagarkar and Das (1993); T. gangeticus Tripathi (1952); T. kalbensi sp. nov. Singh (2011); Neothelohanellus indicus (Gupta and Khera, 1988) Lom and Dykova, 1992

i3 Labeo dero vern. gid (common name: gid ) 30 10 Thelohanellus deri sp. nov. Singh (2011)

i4 Labeo rohita vern. rohu (common name: rohu) 135 58 Myxobolus patialensis Kaur and Singh (2011a); M. punjabii Kaur and Singh (2010/2011); M. saugati Kaur and Singh (2011f); M. saranae Gupta and Khera (1990); M. stomum Ali et al., (2003); M. sushmii Kaur and Singh (2010/20l1); Thelohanellus rohi sp. nov. Singh (2011)

i5 Mystus seenghala vern. seenghala (common name: seenghala) 30 Nil -

i6 Notopterus notopterus vern. parri (common name: grey featherback) 25 Nil -

i7 Ophiocephalus marulius vern. Sol (common name: giant snake head) 15 Nil -

ia Ophiocephalus punctatus vern. damra (common name: spotted snakehead ) 10 Nil -

i9 Puntius sophore vern. chital, ticker barb (common name: spot fin swamp barb) 25 20 Myxobolus chittalii Kaur and Singh (2011b)

2o Wallago attu vern. mulle (common name: boal, freshwater shark) 114 40 Myxobolus duodenalis Kaur and Singh (2011a); M. szekeli Kaur and Singh (2011f); Thelohanellus batae Lalitha Kumari (1969); T. wallagoi Sarkar (1985)

* Total number of fishes examined = 1.397, total number of fishes infected = 78, total prevalence= 55.8%.

S. No. Host examined Number examined Number infected Organs examined Organs infected Infection in percentage (%) Myxozoan parasites recorded

i Carassius carassius 50 Nil gills, fin, scales, skin, air bladder, gall bladder, body- cavity, eye, stomach, intestine Nil - -

2 Catla catla 35 23 -do- gills, scales 65.7% Myxobolus catli

З Cirrhina mrigala 35 25 -do- gills, fin 71.4% Myxobolus eirasi; M. ropari; M. slendrii; M. venkateshi

4 Colisa lalia 20 Nil -do- Nil - -

Б Ctenopharyngodon idella 70 Nil -do- Nil - -

б Cyprinus carpio 20 Nil -do- Nil - -

7 Eutropiichthys murius 40 Nil -do- Nil - -

а Hypophthalmichths molitrix 20 Nil Nil - -

9 Labeo bata 22 16 -do- gills, fin 72.7% Thelohanellus avijiti

io Labeo dero 30 10 -do- gills, fin 33.3% Thelohanellus deri

ii Labeo rohita 55 40 -do- fin, scales 72.7% Myxobolus patialensis; M. stomum; Thelohanellus rohi

* Total number of fishes examined = 397, total number of fishes infected=114, total prevalence= 28.7%.

and grey feather back (Notopterus notopterus) were examined. A total of 1,158 carps were examined which comprised mola carplet, crucian carp, thail, reba carp, mrigal, grass carp, mirror carp, silver carp, bata, kalbans, gid, rohu, and blackspot barb. Among them 402 carps (9 species) were infected (34.71%) with as many as 40 species of myxosporeans belonging to genera Myxobolus, Thelohanellus, Neothelohanellus and Triangula. In addition to this, a total of 144 catfishes naming seenghala and mulle were examined, 40 were found infected (27.7%) with

4 species of myxozoans (Myxobolus duodenalis, M. szekeli, Thelohanellus batae and T. wallagoi). No infection was found in murrels, gourami, batchwas and grey feather back fishes. The present study indicated that the maximum mean intensity of the parasite species was shown by Myxobolus duodenalis followed by Triangula cirrhini and maximum abundance again by M. duodenalis followed by M. szekeli (Table 5).

Four major carps examined were C. mrigala, L. rohita, Catla catla and L. calbasu. Among these Catla catla was most susceptible to myxozoans (9 species) followed by C. mrigala (8 species), C. reba (8 species), L. rohita (7 species) and L. calbasu (5

species). Kalavati and Nandi (2007) also discussed that out of three major carps in India, the most susceptible was L. rohita, followed by C. mrigala and Catla catla. Furthermore, they reported that the parasite virulence was greater in Catla catla with mortality up to 80-90%.

The present study indicated that gills (45.6%), caudal fin (29.4%), duodenum (5.12%), scales (16.1%), pectoral fin (1.92%), pelvic fin (1.67%), eyeball (1.4%), skin of snout (0.38%) and stomach (0.12%) were infected. However, no infection could be detected in air bladder, gall bladder, coelomic cavities, buccal cavity and muscles beneath skin. Longshaw and co-authors (2005) also made similar findings and reported that majority of infections with Myxobolus sp. were found in the gills in cyprinids. Earlier, to this Martins and co-authors (1999a) also reported 79.2% of infection in the gills of Pacu (Piaractus mesopotamicus) with M. colossomatus and Henneguya piaractus. Kalavati and Nandi (2007) discussed that gill myxoboliosis was the most widely distributed disease infecting various species of carps in many states in India and also reported heavy mortality in Andhra Pradesh during November and December, 2000.

S. No. Host examined Number examined Number infected Organs examined Organs infected Infection in percentage (%) Myxozoan parasites recorded

1 Carassius carassius 10 Nil gills, fin, scales, skin, air bladder, gall bladder, body-cavity, eye, stomach, intestine Nil - -

2 Catla catla 77 60 -do- gills, fin, scales, eyeball, skin 77.9 % Myxobolus magauddi;M. sclerii; Thelohanellus kanjalensis; T. mrigalae; T. thaili

3 Cirrhina mrigala 302 258 -do- gills, fin 85.4% Myxobolus eirasi; M. kanjali; M. naini; M. punjabensis; M. venkateshi

4 Cyprinus carpio 10 Nil -do- Nil - -

5 Eutropiichthys murius 10 Nil -do- Nil - -

6 Hypophthalmichthys molitrix 10 Nil -do- Nil - -

7 Labeo calbasu 60 50 -do- scales, fin, gills 83.3% Thelohanellus caudatus; T. gangeticus; T. kalbensi; Myxobolus filamentosus; M. venkateshi; Neothelohanellus indicus

8 Labeo rohita 40 30 -do- fin, scales 75% Myxoblus punjabii; M. saranae; M. saugati

9 Mystus seenghala 10 Nil -do- Nil - -

10 Notopterus notopterus 10 Nil -do- Nil - -

11 Ophiocephalus punctatus 10 Nil -do- Nil - -

12 Wallago attu 10 Nil -do- Nil - -

* Total number of fishes examined = 559, total number of fishes infected = 398, total prevalence= 71.1%.

During the present study, 4-6 plasmodia were found to be present per scale and 5-7 plasmodia were recorded per fin. Molnar (1997) also reported up to 7 plasmodia of M. squamaphilus per scale in sea bream, Abramis brama.

The present study exhibited 36% infection in carps. Wang and co-authors (2003) and Wu and Wang (1997) reported more than 60% infection in carp fishes in China while Bauer and co-authors

(1991) and Yokoyama and co-authors (1996) reported more than 10% infection rate in carp fishes in Russia and Japan (Tokyo), respectively. In the present study, no infection was found in Cyprinus carpio as also observed by Martin and co-authors (1999a) from Brazilian fishes.

Acknowledgements

The authors express thanks to University Grants Commission (UGC) for the financial support.

References

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S. No. Host examined Number examined Number infected Organs examined Organs infected Infection in percentage (%) Myxozoan parasites recorded

i Amblypharyngodon mola 30 20 gills, fin, scales, skin, air bladder, gall bladder, body-cavity, eye, stomach, intestine gills, caudal fin 66.6% Myxobolus moli

2 Catla catla 60 50 -do- scales, gills 83.3% Myxobolus parsi; Thelohanellus mucousalis; T. boggoti

З Cirrhina reba 50 40 -do- gills, caudal fin, scales 80% Myxobolus kalmani; Triangula cirrhini; T. ludhianae; Thelohanellus globulosa; T. haldari; T. kalavatae

4 Cirrhina mrigala 27 20 -do- gills, caudal fin 74.0% Myxobolus bhadurius; M. mehlhorni; M. harikensis

Б Carassius carassius 20 Nil -do- - - -

б Eutropiichthys murius 20 Nil -do- - - -

7 Labeo bata 15 Nil -do- - - -

а Labeo rohita 40 30 -do- eye-ball, gills, fin, scales 75% Myxobolus sushmii

9 Notopterus notopterus 15 Nil -do- - - -

io Ophiocephalus marulius 15 Nil -do- Nil - -

ii Mystus seenghala 20 Nil -do- - - -

i2 Puntius sophore 25 20 -do- gills 80% Myxobolus chittalii

1З Wallago attu 104 88 -do- fin, wall of duodenum 84.6% Myxobolus duodenalis; M. szekeli; Thelohanellus batae; T. wallagoi

* Total number of fishes examined = 441, total number of fishes infected = 268, total prevalence= 60.8%.

Bajpai R.R.N., Kundu, T.K. and Haldar D.P. 1981. Observations on Myxosoma magauddi n. sp. (Myxosoma: Myxosomatidae), parasite on the gill filaments of Trichogaster fasciatus. Riv. Parasitol. 42, 343-350.

Basu S. and Haldar DP. 2003. Observations on two new thelohanelloid species (Myxozoa: Bivalvulida) from Indian major carps of West Bengal, India. J. Parasit. Appl. Anim. Biol. 12, 15-24.

Bauer O.N., Voronin V.N. and Yunchis O.N. 1991. Infection of the heart in carp caused by Myxobolus dogieli (Myxosporea, Myxobolidae). Angew. Parasitol. 32, 42-44.

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sea bream Sparus aurata L. Bull. Eur. Assoc. Fish Pathol. 12, 64-66.

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Dykova I., Lom J. and Cirkovic M. 1986. Brain myxoboliasis of common carp (Cyprinus carpio) due to Myxobolus encephalicus. Bull. Eur. Assoc. Fish Pathol. 6, 10-12.

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Ranjeet Singh and Harpreet Kaur Table 5. Prevalence of myxozoan parasites in the fishes collected from wetlands of Punjab.*

Genus Site of infection No. of examined fish No. of infected fish No. of collected parasite Prevalence (%) Mean intensity Abundanc (%)

Myxobolus bhadurius Gill lamellae 35 13 117 37.14% 9 3.3

Myxobolus catli Gill lamellae 40 13 117 32.5% 9 2.9

Myxobolus chittalii Gill lamellae 40 13 247 32.5% 19 6.1

Myxobolus duodenalis Inner wall of the duodenum 40 25 5925 62.5% 237 148.1

Myxobolus eirasi Caudal fin 30 25 2800 83% 112 93.3

Myxobolus filamentosus Scales 10 2 88 20% 44 8.8

Myxobolus harikensis Caudal fin (in between fin rays) 45 15 285 33.333% 19 6.3

Myxobolus kalmani Gill lamellae 33 25 425 75.758% 17 12.8

Myxobolus kanjali Scales 40 32 2240 80% 70 56

Myxobolus magauddi Gill lamellae 15 10 560 66.667% 56 37.3

Myxobolus mehlhorni Gill lamellae 25 13 286 52% 22 11.4

Myxobolus moli Gill lamellae 20 1 31 5% 31 1.5

Myxobolus naini Gill lamellae 50 32 224 64% 7 4.4

Myxobolus parsi Scales 35 25 1225 71.4% 49 35

Myxobolus patialensis Caudal fin 110 77 11473 63% 149 104.3

Myxobolus punjabensis Caudal fin 50 38 3838 76% 101 76.7

Myxobolus punjabii Caudal fin 15 5 730 33.3% 146 48.7

Myxobolus roparae Gill lamellae 55 30 510 54.5% 17 9.2

Myxobolus saranae Caudal fin 15 2 54 13.333% 27 9

Myxobolus saugati Scales 62 35 6335 56.4% 181 102.1

Myxobolus sclerii Eye-ball (sclera) 10 3 138 30% 46 13.8

Myxobolus slendrii Gill lamellae 52 12 324 23% 27 6.23

Myxobolus stomum Scales 40 32 2336 80% 73 58.4

Myxobolus sushmii Eye- ball 28 8 1248 28.5% 156 44.5

Myxobolus szekeli Inner wall of the stomach 25 1 8 4% 8 0.3

Myxobolus venkateshi Gill lamellae 25 22 3938 88% 179 157.5

Thelohanellus avjiti Pelvic fin 25 13 286 52% 22 11.4

Thelohanellus batae Wall of duodenum, pectoral fin 20 15 465 75% 31 23.2

Thelohanellus boggoti Gill lamellae 14 3 57 21% 19 4.0

Thelohanellus caudatus Caudal fin 22 13 481 59.091% 37 21.8

Thelohanellus deri Caudal fin 10 2 66 20% 33 6.6

Thelohanellus gangeticus Gill lamellae 20 12 132 60% 11 6.6

Thelohanellus globulosa Caudal fin 15 7 182 46.667% 26 12.1

Thelohanellus haldari Caudal fin 12 3 198 25% 66 16.5

Thelohanellus kalavatae Caudal fin 12 3 78 25% 26 6.5

Thelohanellus kalbensi Gill lamellae 10 2 34 20% 17 3.4

Thelohanellus kanjalensis Skin of snout 10 3 192 30% 64 19.2

Thelohanellus mrigalae Caudal fin 15 7 217 46.6% 31 14.4

Thelohanellus mucousalis Gill lamellae 40 31 465 77.5% 15 11.6

Thelohanellus rohi Caudal fin 42 33 1815 78.571% 55 43.2

Thelohanellus thaili Gill lamellae 50 40 520 80% 13 10.4

Thelohanellus wallagoi Gill lamellae 45 34 442 75.5% 13 9.8

Neothelohanellus indicus Gill lamellae 20 10 70 50% 7 3.5

Triangula cirrhini Gill lamellae 40 17 68 42.5% 4 1.7

Triangula ludhianae Gill lamellae 30 23 207 76.7% 9 6.9

* Total number of fishes examined = 1,397, total number of fishes infected = 780.

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Address for correspondence: Ranjeet Singh, Harpreet Kaur. Department of Zoology and Environmental Sciences, Punjabi University, Patiala-147002, India; e-mail: ranjitsrana@gmail.com; harpreet_bimbra@yahoo.com