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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2016 Sep 15;41(2):305–312. doi: 10.1007/s12639-016-0836-8

Species diversity of the genus Thelohanellus Kudo, 1933 (Myxozoa: Bivalvulida) parasitizing fishes in Indian subcontinent

Harpreet Kaur 1,2,, Ranjeet Singh 2, Anu Katoch 2, Rajni Attri 2, Shoaib Ali Dar 2, Aditya Gupta 2
PMCID: PMC5447613  PMID: 28615831

Abstract

A synopsis of 52 nominal species of the genus Thelohanellus Kudo, 1933 reported to infect freshwater fishes in India is presented. These species infect various organs such as gills, fins, scales, skin, muscles, gall bladder, kidney etc. The diagnostic features of the genus include tear-shaped myxospores with smooth shell valves and single polar capsule. The members are histozoic in their nature of parasitism infecting fresh water fishes. The present manuscript is aimed to compile the list of reported species in India along with essential information on morphometrics of vegetative stage, host, organ preference and pathogenic effects if any. Maximum number of species are recorded from state of West Bengal (25) followed by 23 in Punjab (out of which 8 were already reported from other states of India), Andhra Pradesh (7), Orissa (3), Manipur (1) and Haryana (1). Majority of the species have been recorded to infect major and minor carps (43 species) and 9 species in cat fishes. Out of 43 species infecting Indian major carps, T. batae infected the epithelial lining of gill filament of Labeo bata and also the wall of the duodenum and pectoral fin of Wallago attu in Harike Wetland (Punjab). Organ distribution of the species belonging to the genus Thelohanellus indicated that the plasmodia of 27 species were located in the gills, 14 species in the fins, 7 species in the gall bladder, 4 species in muscles and 3 species in kidney, 2 each in scale and skin on the head region and 1 species each in brain, eye, spleen, liver and wall of the duodenum. Recent studies conducted by the authors and also by few earlier studies in West Bengal have documented many species of Thelohanellus to cause serious gill haemorrhagic disease and dermal lesions. Histological studies on the gills of cultured carps in Punjab infected with members of Thelohanellus have indicated that these parasites cause 15–20 % damage to respiratory surface leading to localized loss of function.

Keywords: Thelohanellus, Fresh water fishes, Gills, Indian major carps

Introduction

Thelohanellus Kudo, 1933 is the second most prevalent genus after Myxobolus Butschli, 1882 infecting freshwater fishes in natural and cultured habitat in India. In general, these are mostly histozoic (within the tissues) and rarely coelozoic (in body cavities). The identification of the genus is based on the morphology and morphometrics of myxospores which is a propagative life cycle stage enclosed in pseudocyst/plasmodium. The myxospores typically have single polar capsule placed anteriorly within the tear shaped body(pyriform to broadly ellipsoidal in valvular view, being more slender in sutural view). Members of the genus Thelohanellus Kudo, 1933 are characterized in having shell with smooth valves and single polar capsule. So far 108 nominal species have been recorded throughout the world (Zhang et al. 2013). Lifecycle of only 2 species have been elucidated, T. hovarkai and T. nokolskii (Yokoyama 1997, 1998; Sze´kely et al. 1998; Liyanage et al. 2003). The former species has been reported to cause a serious disease, haemorrhagic thelohanellosis in Cyprinus carpio (Yokoyama et al. 1998). Anderson et al. (2000) confirmed the transmission and production of actinospores in experimentally infected alternate oligochaete host. According to Molnar (1994) some Thelohanellus species possess very strict host and tissue specificity than others and some species occur exclusively in carp fishes (Akhmerov 1955, 1960). Rhee et al. (1990a, b) demonstrated the therapeutic effect of fumagillin dicyclohexylamine salt for the treatment and prevention of T. kitauei. More recently, real-time quantitative PCR have been used by Cavander et al. (2004) and Kelley et al. (2006) to identify and rapid assessment of the exposure of Myxobolus cerebralis to sentinel fish. Griffin et al. (2009) also applied real-time PCR assay for detection of Henneguya ictaluri infecting commercial channel catfish ponds. A unique feature was recorded as the presence of macro and micro myxospores in some plasmodia in T. jiroveci (Kundu and Haldar 1981). The present synopsis presents data on 52 nominal species belonging to the genus Thelohanellus infecting fresh water fishes in different states of India (up to 2015). Also, provides information on the state-wise distribution, organ specificity and organ location. Clinical symptomatology and pathogenicity caused by this group of parasites has been documented as per the original description. Globally, there are 108 nominal species of the genus Thelohanellus and is the sixth most speciose myxozoan genus after Myxobolus, Myxidium, Henneguya, Ceratomyxa and Chloromyxum (Zhang et al. 2013).

Species diversity of the genus Thelohanellus in Indian fishes

Earlier, Lom and Dykova (1992) had listed 39 species under the genus, Thelohanellus, recently Zhang et al. (2013) gave synopsis of 108 species all over the world and 40 in Indian fishes. Basu et al. (2006) and Kalavati and Nandi (2007) had listed 32 Indian species. Most recently, Basu et al. (2015) gave summarized compilation of 32 species in India. The present synopsis consists of an account of 52 species infecting Indian fishes.

Prevalence

Singh and Kaur (2012d) reported 55.7 % infection with myxozoans, out of which 16 species of Thelohanellus infecting freshwater fishes in wetlands of Punjab with highest prevalence rate in Cirrhinus mrigala in Kanjali wetland of Punjab. Kaur (2014) reported infestation rate of 34.7 % in wetlands and 26.28 % in aquaculture.The present synopsis on a prominent myxosporean genus would be second in series after one on the genus Myxobolus by Kaur and Singh (2012). Although, many reports of pathogenic species have been made in the past in India, however, no apparent pathogenicity has been seen due to thellohanelloid species by workers in various states of India. Dermal lesion by Myxobolus and Thelohanellus were recorded to be common in the states of Andhra Pradesh and Karnataka (Kalavati and Nandi 2007). The most recent study by Kaur and Katoch (2016) have reported 3 gill infecting Thellohanellus species (T.bifurcata, T.dykovae, T. filli), 1 infecting liver (T. wallagoi) and 2 species infecting fins (T. boggoti, T. kalavatae). The studies conducted by Basu and Haldar (1998, 2003) have shown that hybrid carps were more susceptible to myxozoan infestation and in many instances they prove to be more prone to pathogenic effects leading to heavy mortality in culture systems.

Pathogenicity: In Punjab, as many as 3 species of Thelohanellus T. bifurcata Basu and Haldar (1999); T. dykovi Kaur et al. (2014a); T. filli Kaur et al. (2014b) infecting gills have been recorded to be highly pathogenic in cultured major carps (Kaur and Katoch 2014). All the three species were reported to have large-sized pseudocysts occupying most of the gill lamellae thereby causing total destruction of the respiratory surface (Kaur et al. 2014a, b). Mondal et al. (2014) recorded 12.5 % fin infection in L. rohita with T. caudatus (Pagarkar and Das 1993; Kaur et al. 2015). Recently, Kaur and Katoch (2016) recorded 3 gill infecting Thelohanellus species in two locations i.e. gill lamellae (LV3 type) and gill filament (FV1 type), causing mild to severe histopathological changes.

The development of aquaculture during the last decade have resulted in much greater attention paid to problems posed by parasites and their impact on the fish health leading to constraints in the productivity (Kennedy 1994). In Punjab (India) fish culture is an upcoming industry having 8285 ponds practicing polyculture and myxozoan parasites have been recorded to be as the major pests (Kaur et al. 2013a, b, Kaur et al. 2014a, b, Kaur et al. 2015, Kaur and Katoch 2014, 2016). This synopsis has been compiled in order to emphasis on the 52 Indian thellohenelloid species infesting major and minor carps, and pin pointing the pathogenic ones and symptamotology as per respective studies (Table 1). In India, the genus Thelohanellus (52 species) is the second most speciose after Myxobolus with 138 species as indicated in a synopsis by Kaur and Singh (2012). Out of 52 species 43 have been reported to infect Indian major and minor carps and 9 species from the catfishes (Tables 2, 3). T. batae was reported in the gill filaments of Labeo bata has also been reported from the wall of the duodenum and pectoral fin of Wallago attu in Harike Wetland of Punjab (Table 3; Fig. 1).

Table 1.

A summary of Thelohanellus spp. infecting Indian fishes

Species Host Site of infection Locality Myxospore Polar capsule Number of coils Parietal folds Symptomatology/Pathogenicity Reported by
1 T. andhrae Labeo fimbriatus Gills AP, KR 12.8 × 5 7.0 × 2.2 10–11 5 Not apparent Qadri (1962a)
2. T. anilae Labeo rohita Gills WB 33.3 × 12.8 17.5 × 5.3 10–11 × Not apparent Hemananda et al. (2010a, b)
3. T. auerbachi Tachysurus plastystomus Gall bladder WB 14.8 × 5.3 8.0 × 3.7 5–6 × Not apparent Sarkar (1987)
4. T. avijiti L. rohita, L. bata Dorsal fin WB, PB 14.0 × 9.7 6.0 × 4.0 6–8 × Not apparent Basu and Haldar (2003)
5. T. batae L. bata, Wallago attu Gill filament, Wall of duodenum, Pectoral fin AP, PB 12.3 × 6.2 7.7 × 3.0 4–6 × Not apparent LalithaKumari (1969)
6. T. bengalensis Catla catla Gall bladder WB 10.9 × 6.5 5.4 × 3.4 3–4 × Not apparent Sarkar and Raychaudhuri (1986)
7. T. bifurcata L.rohita × C.catla L. rohita (Cultured) Gills WB, PB 34.8 × 9.2 23.3 × 6.6 15–20 × Mucous laden and pale gills, Necrosis of Intralamellar and intrafilamental tissue Basu and Haldar (1999)
8. T. boggoti L. boggot, C. catla Gill lamellae AP, PB 11.5 × 6.75 6.25 × 3.8 10–11 × Mucous laden gills Qadri (1962b)
9. T. calbasui L. calbasu Scales WB 9.9 × 7.2 5.4 × 3.4 × Not apparent Tripathi (1952)
10. T. caudatus (Acc. No. KC865607) L. rohita, L. calbasu Between the rays of caudal fin anal fin and Caudal fin WB, PB 13.8 × 9.0 6.99 × 5.32 6–7 × Not apparent Pagarkar and Das (1993)
11. T. catlae C. catla Branchiae WB 20.3 × 11.0 12 × 11 9–10 × Not apparent Chakravarty and Basu (1948)
12. T. chanadannagarensis C. catla Gill filament WB 12.5 × 6.7 5.1 × 3.1 8–10 × Not apparent Basu and Haldar (2003)
13. T. chelae Chela bacaila Gall bladder WB 9.8 × 5.5 4.9 × 2.8 5 × Not apparent LalithaKumari (1969)
14. T. chilkensis L. rohita Gall bladder OD 26.7 × 8.7 17.5 × 7.0 6 × Not apparent Kalavati and Vaidehi (1991)
15. T. chrysopomati Barbus chrysopoma Gill contents AP 12.4 × 5.4 6.5 × 2.7 9–10 × Not apparent LalithaKumari (1969)
16. T. coeli Tachysurus tenuispinis Gall bladder WB 12.7 × 7.1 7.13 × 3.2 6–8 × Not apparent Sarkar and Mazumdar (1983)
17. T. deri L. dero Caudal fin PB 10.0 × 5.0 5.4 × 3.6 6–7 × Not apparent Singh and Kaur (2012a, b, c, d)
18. T. dykovi L. rohita (Cultured) Gills PB 10.7 × 4.0 6.4 × 2.0 18–20 × Necrosis of Intrafilamental tissue tissue Kaur (2014)
19. T. endodermitus L. rohita Under surface of scales WB 13.6 × 5.3 7.1 × 3.0 8–12 × Not apparent Mukhopadhyay and Haldar (2004)
20. T. filli L. rohita (Cultured) Gills PB 27.0 × 10.5 16.6 × 8.2 12–14 × Mucous laden gills and Necrosis of Intrafilamental tissue Kaur et al. (2014b)
21. T. gangeticus Chela bacaila, Puntius vittatus, L. calbasu Muscles, Brain tissue, Gill lamellae WB, KR, PB 16.8 × 5.4 7.2 × 2.5 9 × Mucous laden gills Tripathi (1952)
22. T. globulosa Cirrhinus reba Caudal fin PB 11.7 × 7.9 5.3 × 4.8 4–5 × Not apparent Singh and Kaur (2012a, b, c, d)
23 T. habibpuri L. rohita Pectoral fin WB 13.9 × 8.5 6.0 × 4.9 3–4 × Not apparent Acharya and Dutta (2007)
24. T. haldari C. reba Caudal fin PB 12.6 × 6.2 7.0 × 4.8 3–4 × Not apparent Singh and Kaur (2012a, b, c, d)
25. T. imphalensis L. rohita Gills MN 21.2 × 9.3 10.8 × 3.8 7–8 × Not apparent Hemananda et al. (2010b)
26 T. jiroveci L. bata Gills WB Macro: 35.0 × 12.4
Micro: 16.3 × 6.8
Macro: 18.4 × 7.0
Micro: 7.3 × 4.1
10–12 × Not apparent Kundu and Haldar (1981)
27 T. kalavatae C. reba Caudal fin PB 11.5 × 5.0 5.2 × 3.3 5–6 × Not apparent Singh and Kaur (2014)
28. T. kalbensi L. calbasu Gill lamellae PB 9.5 × 4.9 4.8 × 3.2 5–6 × Mucous laden gills Singh and Kaur (2014)
29 T. kanjalensis C. catla Skin of snout PB 11.7 × 6.6 7.5 × 3.3 4–6 × Not apparent Singh and Kaur (2012a, b, c, d)
30 T. lamelliformis C. catla Gill lamellae PB 10.2 × 4.9 3.8 × 2.6 6–7 × Mucous laden gills Singh and Kaur (2015)
31 T. mrigalae C. mrigala, C. catla Skin on the head, WB, PB 11.4 × 6.7 6.3 × 4.3 6–7 × Not apparent Tripathi (1952)
32 T. muscularis (NCBI unpublished, Acc. No. KT387308 Labeo rohita Head muscles PB 9.2 × 4.0 5.8 × 3.10 5–6 × Cystic appearance of muscles Kaur et al. (2015)
33 T. narasimhamurtius Ambylpharyngodon mola Internal lamellae of gill filament WB 9.6 × 3.3 6.5 × 2.2 9–10 × Necrosis of Interlamellar tissue Sarkar (1994)
34 T. neocyprini (NCBI unpublished, Acc. No. KP792568 C. catla Gill filament PB 34 × 9.0 18.5 × 5.8 10–14 × Highly symptomatic Kaur et al. (2015)
35 T. opthalmicus Glossogobius giuris Internal musculature and sclera of eye WB, KR 12.5 × 7.5 6.5 × 3.2 6–7 × Not apparent Haldar et al. (1983)
36 T. orissae C. mrigala Gills OD Macro: 13.8 × 4.8
Micro: 7.2 × 3.1
Macro: 6.3 × 2.3
Micro: 3.7 × 2.3
6 × Not apparent Haldar, Samal and Mukhopadhyay (1997)
37 T. parastromataei Parastromataeus Gall bladder OD 11.1 × 9.4 8.6 × 6.8 × Not apparent Narasimhamurti et al. 1990
38 T. potaili L. potail Fin AP 13.0 × 8.2 5.9 × 4.3 4 × Not apparent LalithaKumari (1969)
39 T. pyriformis Tinca tinca, Rutilus rutilus, Leuciscus idus Gills, Muscles kidney, Spleen, Liver HR (Elsewhere: France, Russia, South East Asia) 17.1 × 7.0 8.2 × 4.2 6 × Massive hypertrophy of the endothelial cells Thelohan (1892), Kudo (1933)
40 T. qadrii L. potail Gill filaments AP 14.7 × 5.4 8.2 × 3.8 13–18 × Not apparent LalithaKumari (1969)
41 T. rodgii L. calbasu Gills WB 34.3 × 11.7 16.9 × 7.6 × Not apparent Hagargi, Kundu and Haldar (1979)
42 T. rohi L. rohita Caudal fin PB 14.5 × 7.7 5.5 × 4.7 4–5 × Not apparent Singh and Kaur (2015)
43. T. rohitae L. rohita, L. bata Gills WB 31.5 × 11.5 18 × 15.5 6 × Not apparent Southwell and Prashad (1918)
44 T. sanjibi Mystus gulio Kidney WB 12.5 × 8.2 4.5 × 4.0 4–5 × Not apparent Sarkar and Ghosh (1990)
45 T. seni (Southwell and Prashad) C. catla Branchiae WB 13.78 × .5 6.4 × 4.5 6 × Not apparent Chakravarty and Basu, 1948 (Syn. Myxobolus seni Southwell and Prashad, 1918)
46 T. shortti L. fimbriatus Fin AP 12.5 × 6.9 7.0 × 4.2 3–4 × Not apparent Qadri (1967)
47 T. sp (NCBI unpublished, Acc. No. KU516661, Labeo dero Gills Caudal fin PB 9.7 × 3.85 3.0 × 2.68 5–6 × Not apparent/Necrosis of gill lamellae Kaur et al. (2015)
48 T. sudevi A. mola Kidney WB 14.0 × 5.8 5.1 × 2.6 4–5 × Not apparent Sarkar and Ghosh (1990)
49 T. thaili C. catla, L. bata Gill lamellae PB 11.6 × 7.2 7.34 × .4 4–5 × Mucous laden gills Singh and Kaur (2012a, b, c, d)
50 T. theinensis (NCBI unpublished, Acc. No KT387307 L.bata Gill lamellae PB 8.3 × 4.4 4.4 × 4.3 5–6 Mucous laden gills Kaur et al. (2015)
51. T. tripurensis Labeo calbasu, Labeo bata, Labeo gonius and Cirrhinus reba Gill filaments Tripura 17.4 × 10.1 6.3 × 4.4 5–6 × Not apparent Madhavan, Bandyopadhyay and Santosh (2012)
52 T. wallagoi Wallago attu Gall bladder, Gill WB, PB 9.2 × 4.8 5.4 × 2.7 4–5 × Mucous laden gills Sarkar (1987)

AP Andhra Pradesh, HA Haryana, MN Manipur, OD Orissa, PB Punjab, KR Kerala, WB West Bengal

Table 2.

Showing list of species recorded

S. no. Host fish Parasite recorded
1 Catla catla vern. thail T. bengalensis; T. catlae; T. chanadannagarensis; T. opthalmicus; T. seni; T. lamelliformis; T. kanjalensis; T. thaili
2 Cirrhinus reba vern. mori T. kalavatae; T. globulosa; T. haldari; T. tripurensis
3 Cirrhinus mrigala vern. mrigal T. disporomorphus; T. mrigalae; T. orissae
4 Labeo bata vern. bata T. batae; T. jiroveci; T. rohitae; T. thaili; T. theinensis; T. tripurensis
5 Labeo calbasu vern. kalbans T. calbasui; T. kalbensi; T. rodgii; T. tripurensis
6 Labeo dero vern. gid T. deri
7 Labeo rohita vern. rohu T. anilae; T. caudatus; T. chilkensis; T. dykovi; T. endodermitus; T. filli; T. habibpuri; T. rohi; T. imphalensis; T. avijiti; T. rohitae, T. bifurcate; T. muscularis
8 Labeo potail vern. hoobli T. potaili; T. qadri
9 Labeo fimbriatus vern. tambir, rachu T. andhrae; T. shortii
10 Labeo boggot vern. boggut T. boggoti
11 Labeo rohita x L. bata (hybrid) T. rohitae; T. thaili, T.bifurcata
12 Ambylpharyngodon mola vern. molacarplet T. narasimhamurtius; T. sudevi
13 Tinca tinca vern. golden tench T. pyriformis
Table 3.

Species of the Genus Thelohanellus Kudo, 1933 infecting non-major and minor carps in India

S. no. Host fish Parasite recorded
1 Wallago attu vern. mully T. batae; T. wallagoi
2 Chela bacaila vern. katari T. chalae; T. gangeticus
3 Barbus chrysopoma vern. olive barb T. chrysopomati
4 Tachysurus tenuispinis vern. etta T. coeli
5 Mystus guliovern long whiskers catfish T. sanjibi
6 Parastromataeus niger vern. black pomfret T. parastromataei
7 Tachysurus plastystomus vern. flatmouth catfish T. auerbachi
Fig. 1.

Fig. 1

Organ-wise distribution of the species of the genus Thelohanellus Kudo, 1933 in the fresh water fishes of India

Organ distribution

The plasmodia of 27 species were located in gills, 14 species in fins, 7 in gall bladder, 4 species in muscles and 3 species in kidney, 2 species each in scales and skin on head, 1 each in eye, brain, spleen, liver and wall of duodenum.

Molecular data on Indian species of Thelohanellus

The systematic of Thelohanellus spp. is primarily based on the morphology and morphometrics of the myxospore, type host and tissue location however recently molecular study based on partial amplification of SSU rDNA on 14 Indian species have been done as per the data in NCBI GenBank. These are- T. caudatus Acc. No. KM865607 (Mondal et al. 2014; publ), T. habibpuri KM252683 (Abraham et al. 2014-NCBI; unpubl.), T. rohitae Acc. No. KM252682 (Abraham et al. 2014- NCBI; unpubl.), T catlae Acc. No. KJ476881 (Abraham et al. 2014- NCBI; unpubl.), T. jiroveci Acc. No. KJ476885 (Abraham et al. 2014- NCBI; unpubl.), T. seni Acc. No. KJ476884 (Abraham et al. 2014-NCBI; unpubl.), T. quadrii Acc no. KF170928 (Banerjee et al. 2015; publ), T. bifurcata Acc. No. KJ476886- NCBI; unpubl.), T. dykovae Acc. No. KR423868 (Attri and Kaur, 2015-NCBI; unpubl.), T. neocyprini Acc. No. KP792568 (Kaur et al. 2015- NCBI; unpubl.), T. filli Acc. No. KR340464 (Kaur et al. 2015; publ.) and T. theinensis Acc. No. KT387307 (Kaur et al. 2015- NCBI; unpubl.), T. muscularis (Kaur et al. 2015- NCBI; unpubl.),

Thelohanellus sp. Acc. No. KU516661 (Kaur et al. 2015- NCBI; unpubl.).

Conclusions

This synopsis has been compiled in order to emphasis on the 52 Indian thellohenalloid species infesting major and minor carps, and pin pointing the pathogenic ones. In future, this data would form the basis of molecular identification of those species which are morphologically resemble closely recorded from same geographical area.

Acknowledgments

The authors acknowledge financial support by DST–Purse Grant sanctioned to Department of Zoology, Panjab University, Chandigarh.

Author contributions

The corresponding author is supervising subsequent authors who are persuing PhD/PDF under her guidance.

Compliance with ethical standards

Conflict of interest

No conflict of interest.

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