REVIEW ARTICLE

A taxonomic revision of some previously described speciesof monogenoideans found on Indian Siluriform fishes

Priyanka Tripathi • Nirupama Agrawal

Received: 1 April 2013 / Accepted: 10 September 2013

� Indian Society for Parasitology 2013

Abstract A Taxonomic revision of. Bychowskyella bag-

ariusi Sharma, 1983 and Bychowskyella singhi Rajeshwari

& Kulkarni, 1983 Jain, 1952 found on Indian Siluriform

fishes is being done in the present work. These species

were considered as species inquirenda or nomen nudum,

(Lim et al. Syst Parasitol 50:159–197, 2001) and thus, their

taxonomical clarification was required Among them, B.

bagariusi Sharma, 1983 from Bagarius bagarius (Hamil-

ton) is considered as valid and B. singhi Rajeshwari &

Kulkarni, 1983 from Wallago attu (Bloch & Schneider),

belongs to the genus Thaparocleidus Jain, 1952.

Keywords Bychowskyella � Status � Wallago attu �Misidentification � Revision

Introduction

The genus Bychowskyella Achmerov (1952) (syns: Sil-

onditrema Tripathi; Sprostonia Jain; Neosprostonia Jain;

Clariotrema Long; Neobychowskyella Ma, Wang & Li)

was established by Achmerov (1952) with Bychowskyella

pseudobagri Achmerov, 1952 as its type species from ba-

grid fishes of the Amur-Chinese region of China. To date,

this genus comprises 32 species, reported from South East

Asia, parasitizing 28 catfish species of 15 general Lim et al.

(2001). Among these, 22 species have been reported from

India; infesting cat-fishes of the families: Clariidae, Silu-

ridae & Sisoridae of the order Siluriformes.

During the present investigation on monogenoidean

parasites of Indian Siluriforme fishes, it was understood

that diagnosis of some previously described species of

Bychowskyella is incomplete, as it is primarily based on

illustration of hard parts alone. Some were misidentified at

generic and specific level based on minor morphological

variations, demanding further examination of type speci-

mens. Also, in almost all the cases, the type-material was

either in poor condition or not available. In addition, (Lim

et al. 2001), in their exhaustive review of monogenoidean

parasites of siluriform fishes from Old World, considered

only 17 Indian species of Bychowskyella as valid and five

species either species inquirenda or nomen nudum

(Table 1). This paper reviews the taxonomy of Indian

species of Bychowskyella. The genus Bychowskyella is

characterized by the presence of three pairs of hooks with

dilated proximal handles (henceforth referred to as large

hooks) others of larval types (henceforth referred to as

small hooks) and two additional rodlike sclerites one on

either side of dorsal anchors; two dorsal anchors without

roots, stout base, long shaft, long recurved patches; two

ventral anchor without roots, with stout base, dorsal con-

nective bar almost straight, fenestrated in middle and,

ventral bar paired (Lim et al. 2001).

Materials and methods

The hosts fishes were collected from Gomti River, Luc-

know and adjoining areas. The worms, collected from gills,

were studied mostly live under a phase contrast microscope

or after being fixed in 3 % formalin diluted with lukewarm

water. The methods of staining, mounting, and illustrating

P. Tripathi (&) � N. Agrawal

Department of Zoology, University of Lucknow, Lucknow

226007, Uttar Pradesh, India

e-mail: Priyankatripathi24@gmail.com

N. Agrawal

e-mail: dr_neeru_agrawal@yahoo.co.in

123

J Parasit Dis

DOI 10.1007/s12639-013-0359-5

the dactylogyrids were based on Kritsky et al. (1986).

Measurements were taken using a calibrated micrometer,

and are given in micrometers (lm) with the mean followed

by the range and the number (n) of specimens measured in

parentheses. Unstained, unflattened specimens were used to

obtain the measurements of the internal organs (pharynx

and gonads), the body and the haptoral sclerites. Illustra-

tions were prepared with the aid of a camera lucida

attached to a phase-contrast microscope. Host name fol-

lows FishBase (Froese and Pauly 2007).

Voucher specimens were deposited in the ZSI, Kolkata.

Results

Class Monogenoidea Bychowsky, 1937

Order: Dactylogyridea Bychowsky, 1937

Fam: Dactylogyridae Bychowsky, 1933

Genus: Bychowskyella Achmerov, 1952

Species: Bychowskyella bagariusi Sharma, 1983

(Figs. 1, 2–8b)

Table 1 List of Indian species of the genus Bychowskyella (Lim

et al. 2001)

Indian species of the genus

Bychowskyella

Status Hosts

B. asiatica (Jain, 1959) Gusev, 1961 Valid Ompok pabda (Ham.

1822)

B. wallagonia (Jain, 1959) Gusev,

1961

Valid Wallago attu (Bl.&

Sch., 1801)

B. gomtia (Jain, 1959) Gusev, 1961 Valid Eutropiicthyes vacha

(Ham. 1822)

B. indica (Jain, 1959) Gusev 1961 Valid Eutropiicthyes vacha

(Ham. 1822)

Syn: B.garuai (Agrawal &Singh,

1982) Agrawal & Sharma, 1990

Clupisoma.garua

(Ham. 1822)

B. gharui (Tripathi, 1959) Gusev,

1961

Valid Lupisoma.garua

(Ham. 1822)

Syn: B. gussevi Majumdar &

Agarwal, 1989

Clupisoma.garua

(Ham. 1822)

B. vacha (Tripathi, 1959) Gusev,

1961

Valid E. vacha (Ham.

1822)

Syn: B. lucknowensis Agrawal &

Sharma, 1990

– E. vacha (Ham.

1822)

B. cauveryi (Tripathi, 1959) Gusev,

1961

Valid Silonia silondia

(Ham. 1822)

B. bychowskii Gusev, 1977 Valid Pseudotropius

takree

B. caballeroi Gusev, 1977 Valid C.garua (Ham. 1822)

B. chauhani Venkatanarsaiah, 1989 Valid W. attu (Bl.& Sch.,

1801)

B. raipurensis Majumdar & Agarwal,

1989

Valid Rita-rita (Ham.

1822)

B. pricei Majumdar & Agarwal, 1989 Valid C. garua (Ham.

1822)

B. fossilisi Majumdar & Agarwal,

1989

Valid Heteropneustes

fossilis (Bloch,

1794)

B. kanpurensis Agrawal, Shukla &

Vishwakarma,1996

Valid Ompok bimaculatus

(Bloch, 1794)

B. jaini Agrawal, Shukla &

Vishwakarma,1996

Valid C. garua (Ham.

1822)

B. tchangi Gusev, 1976 Valid Clarius batrachus

B. tripathii Kumar & Agrawal, 1981

[originaly ntioned as Silonditrema

tripathai Kumar & Agrawal,

1977 nomen nudum]

Valid W. attu (Bl.& Sch.,

1801)

B. bagariusi Sharma, 1987 Sp.Inq. Bagarius bagarius

(Ham., 1822)

B. singhi Rajeshwari & Kulkarni,

1983

Sp.Inq. W. attu (Bl.& Sch.,

1801)

Silonditrema kanpurensis Gupta &

Sachdeva, 1986

Sp.Inq. Mystus tengara

(Ham. 1822)

Silonditrema ritai Gupta, 1986 Sp.Inq. Rita-rita (Ham.

1822)

Neosprostonia garuai Agrawal &

Singh, 1982

Sp.

Inq.

C. garua (Ham.

1822)

Fig. 1 Bychowskyella bagariusi Sharma, 1987 (ventral view)

J Parasit Dis

123

Previous host record and locality: Host: The Devil cat-

fish or dwarf goonch, Bagarius bagarius (Hamilton) (Si-

luriformes: siluridae), Locality: River Yamuna, Etawah,

U.P., India.

Infection site: Gills.

Present host record, additional locality & collection

dates: Host: Bagarius bagarius (Hamilton), Locality; River

Sharda,

Lakhimpur Khiri, India (27�50 83–28�60^N; 80�340–81�300E)

River Gomti, Lucknow, India (26�450 84–27�N;80�500

85–81�050E)

Number of parasite specimens examined: 10

Specimens deposited: Voucher specimens W9370/1,

W9376/1-W9378/1 in ZSI, Kolkata.

Redescription: Body length370 (350–380; n = 10);

maximum width 120 (110–125; n = 10) at mid-length of

body. Cephalic region well developed; four cephalic lobes.

Two pairs of eye spots, posterior pair larger, accessory

granules absent. Pharynx spherical, 22 (20–25; n = 10) in

diameter; oesophagus short to non-existent.

Testis 30 (25–35; n = 8) long, 12 (10–14; n = 8) wide;

vas deferens loops left intestinal caecum; two seminal

vesicle, a sigmoid dilation of vas deferens, present. Two

Prostatic reservoirs present. Copulatory complex consists

of a copulatory tube, proximally articulating accessory

piece. Copulatory tube sclerotised, 45(40–47; n = 10)

long. Accessory piece, divided into two pieces, 60(55–65;

n = 10) long. Ovary round to oval, long, intercaecal; ovi-

duct, ootype, uterus not observed. Seminal receptacle,

vaginal armament not observed. Vitellaria dense,

throughout trunk, except in regions of reproductive organs.

Haptor 120 (110–125; n = 10) long, 140 (135–145;

n = 10) wide. Dorsal anchor, inner length 60 (55–65;

Figs. 2–8b Bychowskyella

bagariusi Sharma, 1987. 2Dorsal anchor. 3 Patch. 4Ventral anchor.5 Ventral bar. 6Dorsal bar. 7 Hooks. 8Onchium. 8a Sclerite. 8bCopulatory complex

J Parasit Dis

123

n = 10), recurved point 22 (20–25; n = 10) long, Patch 50

(46–54; n = 10), Ventral anchor: inner length 34 (30–36;

n = 10), recurved point 22 (20–25; n = 10) long, outer and

root having facets. Dorsal connective bar fenestrated 72.

(70–75; n = 10) long, Ventral bar, 57 (55–58; n = 10)

long. Serrated onchium, 30(28–32; n = 10) long. Sclerite,

35 (32–36; n = 10) long. Seven pairs hooks. Three pairs

with dilated proximal handles, others are of larval type

with dimensions as follows-: pair 2, 6, 5 and 7 larval types:

10 long, pairs 1 and 4:50 long; pair 3:38 long.

Remarks: Bychowskyella bagariusi was described by

Sharma (1983) from river Yamuna at Etawah, Uttar Pradesh

from the gills of Bagarius bagarius. Lim et al. (2001) con-

sidered it as species inquirenda. Our collection and study of

specimens from the type host, revealed it to be a valid spe-

cies. In the present specimens, the outer and inner root of

ventral anchor, having small facets has been recorded for the

first time. The patches on dorsal anchors were wrongly

designated as accessory bars. The intestinal caeca were

confluent. Sharma (1983) recorded only six pairs of hooks

instead of seven in the specimens. Serrations on onchium, a

unique feature, was not recorded earlier in the species.

Complicated structure of accessory piece of copulatory

organ is also well illustrated in the present study.

Class Monogenoidea Bychowsky, 1937

Dactylogyridea Bychowsky, 1937

Dactylogyridae Bychowsky, 1933

Thaparocleidus Jain, 1952.

Thaparocleidus indicus (Kulkarni 1969) Lim, 1996.

Syn.: Bychowskyella singhi Rajeshwari and Kulkarni,

1983. (Figs. 9, 10–16).

Previous record and locality: Padhan, Wallago attu

(Bloch & Schneider). (Siluriformes: Siluridae) from.

Hyderabad.

Infection site: Gills.

Present record and locality: W. attu (Bloch & Schnei-

der), river Gomti, Lucknow, India (26�450 84–.

27�N;80�500 85–81�050E).

Number of specimens examined: 15.

Specimens deposited: Voucher specimens W9371/1,

W9379/1 & W9380/1 in ZSI, Kolkata.

Redescription: Body 1,000 (990–1010; n = 10) long;

maximum width 120 (110–125; n = 10) at mid-length.

Cephalic region well developed; four cephalic lobes. Two

pairs of eye spots, posterior pair larger, accessory granules

absent. Pharynx spherical, 22 (20–24; n = 10) in diameter;

oesophagus short to non-existent. Testis 60 (58–62; n = 8)

long, 45 (42–47; n = 8) wide; vas deferens loops left

intestinal caecum; seminal vesicle a sigmoid dilation of vas

deferens. Prostatic reservoir (s) not observed. Copulatory

complex consists of a ‘spicule-like’ copulatory tube and

proximally articulating ‘spicule- like’ accessory piece.

Copulatory tube sclerotised, 58 (5560; n = 13) long.

Accessory piece, 61 (58–62; n = 13) long. Ovary round to

oval, long, intercaecal; oviduct, ootype, uterus not

observed. Seminal receptacle not observed. Vaginal

armament 35 (33–36; n = 5). Vitellaria dense, throughout

trunk, except absent in regions of reproductive organs.

Haptor 75 (72–77; n = 10) long, 125 (122–127;

n = 10) wide. Dorsal anchor: outer length 45 (43–46;

n = 10) Dorsal anchor: inner length 35 (33–36; n = 10),

recurved point 15 (13–16; n = 10) long, Patch 11 (8–13;

n = 10), Ventral anchor: inner length 30 (26–33; n = 15),

recurved point 14 (12–16; n = 10) long, Ventral anchor:

outer length 40 (35–45; n = 10). Dorsal connective bar,

transverse shaft like, lacking a fenestration, 43 (40–45;

n = 14) long, Ventral bar, ‘‘V- shaped’’, 25 (22–27;

n = 13) long, Seven pairs of similar shape and size 14

(12–16; n = 10) hooks.

Remarks: Bychowskyella singhi was described by Ra-

jeshwari and Kulkarni (1983) from the gills of W. attu at

Hyderabad. Lim et al. (2001) considered it as species in-

quirenda. We have collected this species on the type host,

from an additional locality and studied in detail. We com-

pared our specimens with the original descriptions as the

types were not available for study (not deposited by earlier

Fig. 9 Thaparocleidus indicus Kulkarni, 1969 (ventral view)

J Parasit Dis

123

workers). The present study revealed it to be a species of

Thaparocleidus (as pointed out by Lim 2001) because the

dorsal bar of B. singhi, lacked central fenestration (a generic

feature of Bychowskyella); patches on dorsal anchors are

long and recurved in Bychoskyella, while those of B. singhi

are very small; 1st, 3rd and 4th hooks are with dilated

proximal handles and 2nd, 6th, 5th and 7th are of larval type

in Bychowskyella while in B. singhi, all hooks are of variable

shapes and sizes (a character of the genus Thaparocleidus.)

Present study has, therefore, revealed it to be Thaparocleidus

indicus (Kulkarni 1969) Lim, 1996, owing to the ‘spicule-

like’ copulatory complex, ‘V-shaped’ ventral bar, and ‘shaft-

like’ dorsal connective bar.

Discussion

Misidentification and misinterpretation of monogenetic

parasites often creates problems in their taxonomy leading to

incorrect phylogenies. Owing to the confusion prevailing in

India regarding these parasites, where types have almost

never been, properly deposited or made available to taxon-

omists, problems like this needs to be focused upon. Thus, for

correct evolutionary studies, proper identification and

authenticity of these parasites is of utmost importance. By-

chowskyella species possesses three pairs of large hooks and

four pairs of small hooks and two additional rod-like sclerites

one on either side of dorsal anchors (Lim et al. 2001). Genus

Bychowskyella Achmerov, 1952 has 17 valid species as lis-

ted by Lim 2001 in India. Based on present study, B. baga-

riusi is valid and B. singhi Rajeshwari & Kulkarni 1983

belongs to the genus Thaparocleidus Jain 1952.

Acknowledgments The work was supported by grant (No C.S.T./

AAS/D-03) from the Council of State & Technology, U.P.

References

Akhmerow AKh (1952) New species of monogenetic trematodes of

Amur fish. Parazitol Sbornik 14:181–212

Figs. 10–16 Thaparocleidus

indicus (Kulkarni 1969) Lim,

1996. 10 Dorsal anchor. 11Ventral anchor. 12 Dorsal bar.

13 Ventral bar. 14 Vagina. 15Hooks. 16 Copulatory complex

J Parasit Dis

123

Froese R.D and Pauly (2007) Fish base, World wide web electronic

publication. Available from:www.fishbase.org , version (Acces-

sed: 2007 Mar)

Jain SL (1952) Monogenea of Indian freshwater fishes. II.

Thaparocleidus wallagonius n.g. n.sp., (subfamily:Tetraonchi-

nae), from the gills of Wallagonia attu (Bloch). Ann Zool

2:57–62

Kritsky DC, Thatcher VE, Boeger WA (1986) Neotropical Monoge-

nea. 8. Revision of Urocleidoides (Dactylogyridae, Ancyroceph-

alinae). Proceed Helminthol Soc Wash 53:1–37

Kulkarni T (1969) On a new species of Ancylodiscoides Yamaguti,

1937 from the fish Wallagonia attu (Bloch) in Hyderabad, A.P.

Zool Anz 182:462–465

Lim LHS (1996) Thaparocleidus Jain, 1952, the senior synonym of

Siluridiscoides Gussev, 1976 (Monogenea : Odiscoidinae). Syst

Parasitol 35:207–215

Lim LHS, Timofeeva TA, Gibson DI (2001/02) Dactylogyridean

monogeneans of the siluroform fishes of the Old World. Syst

Parasitol 50:159–197

Rajeshwari JS, Kulkarni T (1983) On a new species Bychowskyella

singhi from the gills of a freshwater fish, Wallago attu from

hyderabad, A.P India. Proceed Ind Acad Parasitol 4:49–53

Sharma RK (1983) A new monogenetic trematode Bychowskyella

bagarius n.sp. from a fresh-water fish, Bagarius bagarius (Ham.)

from Etarwah, Uttar Pradesh. Kanpur Univ Research J (Science),

4:77–79

J Parasit Dis

123