Turkish Journal of Zoology Turk J Zool (2016) 40: 758-764 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Short Communication doi:10.3906/zoo-1507-31

Thaparocleidus gangus sp. nov. (Monogenea: Dactylogyridae) from gill filaments of attu Bloch and Schn., 1801,

Chandni VERMA*, Anshu CHAUDHARY, Hridaya Shanker SINGH Molecular Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, India

Received: 24.07.2015 Accepted/Published Online: 11.03.2016 Final Version: 24.10.2016

Abstract: The examination of gill parasites from the freshwater shark Bloch and Schn., 1801 (Siluriformes: ) in India revealed the presence of a new species of the Thaparocleidus Jain, 1952 from the Ganga River, Uttar Pradesh, India. The new species can be discriminated from its congeners by the combination of the following characteristics: accessory piece much smaller than cirrus tube, dorsal anchor with well-developed inner root and small outer root, shaft smoothly bent to form recurved point, inner and outer roots of ventral anchors developed equally so that attain almost equal length, dorsal bar curved in the medial part with expanded lateral ends slightly curved in posterior direction, ventral bar narrowly V-shaped. Thaparocleidus gangussp. nov. was found to be closely related to T. indicus and T. sudhakari as indicated by their similar morphological appearance. It is a larger worm than T. indicus and T. sudhakari species and can further be separated from them by means of the comparative morphology of the anchors, bars, and cirrus.

Key words: Monogenea, Thaparocleidus spp., morphology, Meerut, India

The genus Thaparocleidus was erected by Jain in kao Lim and Lerssutthichawal (1996), from the same host 1952 to accommodate the new species Thaparocleidus in . The present communication deals with the wallagonius Jain, 1952 from the gill filaments of the description of a new species of Thaparocleidus from the freshwater shark Wallago attu (Siluriformes), collected gill filaments of W. attu from Meerut, Uttar Pradesh, India. from Lucknow, Uttar Pradesh, India. This genus was Specimens were collected from the freshwater shark synonymized as Silurodiscoides by Gusev (1976). This fish W. attu during 2011 and 2012 from the Ganga River, genus was again revived as Thaparocleidus by Lim (1996), near Meerut (29°01′N, 77°45′E), Uttar Pradesh, India. The representing Silurodiscoides as the junior synonym. The fish were bought from the market, sometimes directly synonyms of genus Thaparocleidus now include Jainius from fishermen, and identified following Froese and Pauly Akhmerov (1964), Neomurraytrema Tripathi (1959), (http://www.fishbase.org/). Helminthes were stained Parancylodiscoides (Akhmerov, 1964) Caballero and with acetocarmine, dehydrated with ascending grades of Bravo-Hollis (1961), Silurodiscoides Gusev (1976), and alcohol, and mounted in Canada balsam for visualization Wallagotrema Tripathi (1959). The genus Thaparocleidus and measurement of soft internal structures. For the study shows the richest species diversity among the members of of sclerotized structures, the specimens were mounted the Ancylodiscoididae (Lim et al., 2001) infecting silurid in glycerin. Measurements were made according to the fishes. procedure of Gusev (1973), all in millimeters. The average Thaparocleidus spp. are limited to the freshwater measurement is followed by ranges given in parentheses. siluriforms and occur rarely in other groups. The genus The greatest measurement is given for dimensions is characterized by having both pairs of anchors (dorsal of organs and for curved or bent structures; length anchors usually larger than ventral ones) with roots of represents the straight-line distance between extremities. variable length, the presence of a patch on the dorsal Line drawings were prepared with a camera lucida and anchor, complete ventral bar (in some species it has a weak microphotographs of specimen slides were taken using an medial part), and the larval type of marginal hooks. To Olympus CH30 microscope fitted with an AxioCam ERc date, 17 nominal species of Thaparocleidus (Table 1) have 5s. The comparative measurements are given in Table 2. been described from W. attu in India plus one species, T. The morphotypes used in describing species according * Correspondence: [email protected] 758 VERMA et al. / Turk J Zool

Table 1. List of localities, sites, references, and Thaparocleidus spp. extracted from the host Wallago attu in India.

Thaparocleidus spp. Locality Site Reference

T. wallagonius Gomti River, Lucknow Gill filaments Jain, 1952 Haplocleidus gomtius (=Thaparocleidus gomtius) Gomti River, Lucknow Gill filaments Jain, 1952 T. longicirrus Gomti River, Lucknow Gill filaments Tripathi, 1959 Ancylodiscoides indicus (=Thaparocleidus indicus) Hyderabad, Andhra Pradesh Hyderabad, Andhra Gill filaments Kulkarni, 1969 T. isostylus Pradesh Gill filaments Kulkarni, 1969 T. yogendrai Lucknow Gill filaments Agrawal, 1981 T. jaini Lucknow Gill filaments Agrawal, 1981 T. bhagwanpurensis Lucknow Gill filaments Agrawal and Sharma, 1981 T. sohani Lucknow Gill filaments Pandey and Mehta, 1986 T. guptai Lucknow Gill filaments Pandey and Mehta, 1986 T. kherai Lucknow Gill filaments Pandey and Mehta, 1986 T. dayali Lucknow Gill filaments Pandey and Agrawal, 1989 T. surendrai Lucknow Gill filaments Pandey and Agrawal, 1990 T. saharanpurensis Lucknow Gill filaments Pandey and Agrawal, 1990 T. gussevi Meerut Gill filaments Singh et al., 1992 Silurodiscoides vistulensis Meerut Gill filaments Rastogi et al., 2008 T. longiphallus Meerut Gill filaments Chaudhary and Singh, 2013

Table 2. Comparative measurements of T. gangus sp. nov. All measurements are given in millimeters.

Body features T. sudhakari Gusev, 1973 T. indicus Kulkarni, 1969 T. indicus Lim, 1996 T. gangus sp. nov. Body Length 0.50 1.100 0.860–1.400 1.702 (1.695–1.709) Width 0.15 0.030 0.171 (0.150–0.190) 0.195 (0.186–0.204) Pharynx Diameter 0.019 (0.018–0.021) 0.076 (0.074–0.080) – 0.056 (0.055–0.057) Haptor Length 0.096 (0.095–0.098) 0.115 (0.110–0.120) 0.217 (0.150–0.260) 0.181 (0.170–0.193) Width 0.081 (0.079–0.081) 0.163 (0.060–0.169) 0.255 (0.160–0.300) 0.061 (0.110–0.113) Dorsal anchor Inner length 0.046–0.050 0.043–0.045 0.050 (0.048–0.050) 0.048 (0.044–0.052) Outer length – – 0.039 (0.036–0.040) 0.037 (0.034–0.041) Main part 0.010–0.013 0.033–0.040 – 0.039 (0.035–0.044) Inner root – 0.012–0.016 0.015 (0.013–0.018) 0.012 (0.012–0.013) Outer root – 0.002–0.003 – 0.003 (0.003) Recurved point 0.025–0.028 0.022–0.024 0.028 (0.025–0.030) 0.030 (0.026–0.034) Dorsal bar Length 0.020–0.028 0.043 0.039 (0.038–0.043) 0.039 (0.033–0.046) Width 0.003–0.006 0.007–0.009 0.005 (0.005–0.006) 0.008 (0.005–0.011) Dorsal patch Length 0.010–0.015 0.008 0.009 (0.008–0.013) 0.011 (0.009–0.013) Width 0.005–0.006 0.005 0.005 0.004 (0.004–0.005) Ventral anchor Inner length 0.021–0.024 0.045–0.046 0.032 (0.030–0.038) 0.030 (0.027–0.033) Outer length – – 0.037 (0.035–0.040) 0.029 (0.027–0.032) Main part 0.018–0.020 0.029 – 0.026 (0.024–0.029) Inner root 0.003–0.005 0.008 0.009 (0.006–0.013) 0.008 (0.007–0.009) Outer root 0.002–0.004 0.014 0.012 (0.010–0.015) 0.005 (0.005) Recurved point 0.013–0.015 0.016 0.018 (0.015–0.020) 0.018 (0.016–0.021) Ventral connective bar Length Width – – 0.024 (0.021–0.028) 0.023 (0.022–0.024) Hooks – – 0.003 (0.003–0.004) 0.003 (0.003) Total length Sickle 0.014–0.021 0.014–0.015 0.017 (0.016–0.017) 0.021 (0.020–0.022) Handle – – – 0.008 (0.007–0.010) Shaft – – – 0.013 (0.012–0.015) Copulatory complex – – – 0.015 (0.014–0.016) Cirrus tube length 0.040–0.058 0.051–0.053 0.036 (0.030–0.040) 0.074 (0.071–0.076) Accessory piece 0.030–0.040 0.009 0.049 (0.045–0.053) 0.031 (0.029–0.033)

759 VERMA et al. / Turk J Zool to Gusev (1973) include the following: wunderoid-type 0.033) (Figure 1b). Ovary pear-shaped, pretesticular, indicates anchors with sharply recurved almost straight equatorial, and intercecal, 0.109 (0.101–0.115) × 0.077 point and comparatively small root diverging at an angle (0.071–0.084). Vagina and egg not found. not more than 90°; boreal-type indicates anchors having Opisthohaptor elongated, fairly set off from the body inner and outer roots of equal length; anchoratoid proper by a short peduncle. It measures 0.181 (0.170–0.193) wegeneri-type indicates bar with recurved point having × 0.061 (0.110–0.113). Haptoral armature composed of very long inner root but almost without outer root; initial- 2 pairs of anchor (dorsal and ventral), dorsal transverse type indicates copulatory complex having straight or bar, ventral connective bar, and 7 pairs of marginal hooks. curved cirrus tube with widened initial part, accessory Dorsal pair of anchors wunderoid-type with well-defined piece like sticky tape connected with the initial part of base, outer root comparatively much smaller than inner the cirrus tube and directed along it, usually finished by one. Measurements include: inner length 0.048 (0.044– extension; larval-type hooks indicate hooks with handles 0.052), outer length 0.037 (0.034–0.041), main part 0.035– like rounded swellings at the end of the shaft. 0.044 (0.039), inner root 0.012 (0.012–0.013), outer root Family Dactylogyridae Bychowsky, 1933 0.003, recurved point 0.030 (0.026–0.034) (Figure 1c). Genus Thaparocleidus Jain, 1952 Straight and tapering shaft terminates smoothly to bent Thaparocleidus gangus sp. nov. recurved point. Sleeve sclerite present at the midlength of Type host: Wallago attu Bloch and Schn., 1801 shaft and reaches up to the beginning of recurved point. (Siluriformes: Siluridae). Supporting patches small and rectangular in shape, 0.011 Type locality: Meerut (29°01′N, 77°45′E), Uttar (0.009–0.013) × 0.004 (0.004–0.005), present at the base Pradesh, India. of each pair of dorsal anchors (Figure 1c). Dorsal anchors Site of infection: Gill filaments. connected with each other by dorsal transverse bar of Type material: Voucher specimens of Thaparocleidus anchoratoid wegeneri-type measuring 0.039 (0.033–0.046) gangus sp. nov. are deposited in the Museum of the × 0.008 (0.005–0.011), which is slightly curved in the Department of Zoology, Chaudhary Charan Singh medial part and rounded at the lateral ends (Figure 1c). University, Uttar Pradesh, India (Voucher No. HS/ The ventral pairs of anchors comparatively smaller than monogenea/2015/05). dorsal pairs as found in other groups. Ventral anchors Description (n = 3). Body very long with rounded boreal-type in which both inner and outer roots develop anterior and elongated posterior end. Worms measure equally, so they attain almost equal length (Figure 1d). 1.702 (1.695–1.709) in length and 0.195 (0.186–0.204) in Measurements include: inner length 0.030 (0.027–0.033), maximum width attained at the midregion of the body outer length 0.029 (0.027–0.032), main part 0.026 (0.024– (Figure 1a). Head organs not visible clearly at prohaptor. 0.029), inner root 0.008 (0.007–0.009), outer root 0.005 Above pharynx 2 pairs of eye spots present, made up of (0.005), recurved point 0.018 (0.016–0.021). The shaft is melanistic granules, the anterior pair being smaller than cylindrical and straight with smoothly recurved point. the posterior pair. During mounting, these eye spots were The ventral bar V-shaped, consisting of 2 identical pieces; found to be dispersed. Pharynx small, muscular, rounded, each measures 0.023 (0.022–0.024) × 0.003 (0.003) (Figure 0.063 (0.053–0.074). Esophagus short, bifurcation of ceca 1d). Two pieces joined in such a way that they seem to be takes place posterior to pharynx. Crura extend throughout a single piece. Marginal hooks, larval-type, all are similar the length of the body and unite posteriorly, anterior to in shape and size. Each hook having total length 0.021 haptor. (0.020–0.022), consisting of an elongated handle 0.013 The male reproductive system comprises a single testis, (0.012–0.015), a flattened loop, and a sickle-shaped blade vas deferens, and cirrus. Testis single, elongated, intercecal, 0.008 (0.007–0.010). The sickle filament loop is attached postovarian, postequatorial, and saccular structure at the distal part of the sickle on the ventral side. The measuring 0.205 (0.201–0.210) × 0.108 (0.105–0.111) respective detailed structures are also shown in Figure 2. (Figure 1a). Male copulatory organ simple and initial-type, Remarks. Thaparocleidus gangus sp. nov. is said to be consisting of a cirrus tube and an accessory piece. Cirrus unique among other species of the genus Thaparocleidus tube straight, somewhat curved, weakly narrowed to the Jain, 1952. While determining the parasites, it was found termination, 0.074 (0.071–0.076) (Figure 1b). Accessory that T. gangus sp. nov. shows morphological similarities piece comparatively very small to cirrus tube, looks like with 2 congener species of Thaparocleidus, i.e. T. indicus a conical plate having widened termination 0.031 (0.029– (Kulkarni, 1969) Lim, 1996 and T. sudhakari Gusev, 1973.

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Figure 1. Schematic illustrations of Thaparocleidus gangus sp. nov.: (a) whole mount; (b) copulatory organ; (c) dorsal anchors, dorsal patch, dorsal connective bar, and hooks; (d) ventral anchors and ventral bar. Scale bars: a, 0.2 mm; b–d, 0.012 mm.

Having carefully looked through all the slides found during is a simple chitinous stick without or with weakly curved investigation of helminth fauna of W. attu, we determined surface); 2) in the shape of ventral bar (in T. sudhakari that T. gangus is different from T. sudhakari and T. indicus. (Figure 3e), it is V-shaped, narrowed at middle, seems to be T. gangus (Figure 3a–3c) differs from T. sudhakari by: 1) size a 2-piece bar, each half is S-shaped but present form shows and shape of dorsal patch (in T. sudhakari (Figure 3d), it no weakening at the middle of bar, narrowed V-shape); 3) in

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Figure 2. Microphotographs of Thaparocleidus gangus sp. nov. to show the (a) copulatory complex, (b) dorsal anchor and dorsal patch (at high magnification), (c) dorsal anchor and dorsal patch (at low magnification), (d) ventral bar, (e) dorsal bar and hooks. Scale bars: a, b, d, e, 0.01 mm; c, 0.05 mm. the shape of accessory piece and cirrus tube (in T. sudhakari knobbed lateral ends); 3) inconspicuous outer root of (Figure 3f) cirrus tube is looped or spiral curved). When ventral anchor (in T. indicus (Figure 3h) the outer root is comparing the present form with T. indicus, it differs in long and twice the length of the inner one); 4) in difference the following characteristics: 1) in shape and large size of in the size and shape of copulatory complex (in T. indicus dorsal patch (in T. indicus (Figure 3g), outline is smooth, no (Figure 3i) cirrus tube is spicula-shaped, length of accessory curviness is present unlike T. gangus); 2) in slightly different piece and copulatory tube is almost the same, but T. gangus shape of dorsal connective bar (in T. indicus (Figure 3g) it varies in length of accessory piece and copulatory tube, is slightly concave, thickened at the middle, but the present as the accessory piece is much smaller than the long and form has a wavy outline, is stick-shaped with prominent straight cirrus tube).

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Figure 3. Schematic illustrations of: T. gangus (a) dorsal anchors with supporting patches and dorsal transverse bar, (b) ventral anchors and ventral bar, (c) copulatory complex; T. sudhakari (d) dorsal anchors with supporting patches and dorsal transverse bar, (e) ventral anchors and ventral bar, (f) copulatory complex; T. indicus (g) dorsal anchors with supporting patches and dorsal transverse bar, (h) ventral anchors and ventral bar, (i) copulatory complex. All scale bars: 0.012 mm.

Etymology. The species is named after the River Ganga Identifier (LSID) for this publication is: http://zoobank. in India from where the host was collected. org/urn:lsid:zoobank.org:pub:6779DBAE-ADD2-4162- All considerations made above demonstrate that A46D-BC9457909218 the present form shows characteristic differences with 2 congener species, T. indicus and T. sudhakari. On the basis Acknowledgments of these significant morphological differences, the present This study was partially supported by grants from the form is easily accommodated to the new species of genus UGC (University Grants Commission) India, under the Thaparocleidus Jain, 1952 as T. gangus. Senior Research Fellowship [RGNF; F.14-2(SC)/2010 (SA- III)] to CV and Postdoctoral Fellowship [(F.15-191/2012 Nomenclatural acts (SA-II)] to AC. This work and the nomenclatural acts it contains have been registered in ZooBank. The ZooBank Life Science

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