Digenetic Trematode Parasites in Two Fresh Water Fishes Ophiocephalus Punctatus and Xenentodon Cancila From North West Himalayas

Abstract

The study was conducted during September 2018-August 2019 to study the digenetic trematode infection in fresh water fishes of some of the water bodies viz. Gho-manhasan, Chakrali and Chadwal of Jammu region of J&K union territory  A total of 220 fishes comprising Ophiocephalus punctatus and Xenentodon cancila belonging to families Channidae and Belonidae respectively were examined. A total of 4 digenetic trematode parasites belonging to 4 different families i.e., Euclinostomum heterostomum (Clinostomidae Luhe, 1901); Phyllodistomum tripathi (Gorgoderidae Looss, 1901); Genarchopsis piscicola (Hemiuridae, Luhe, 1901), and Bucephalopsis karvei (Bucephalidae Poche, 1907) were detected. The overall prevalence of digenetic trematode infection was 65.90% and the mean intensity was 3.58. Among these Genarchopsis piscicola showed the highest prevalence (40.38%) with mean intensity 2.95 in the host fish Xenentodon cancila, while in other species the prevalence ranged between 26.23% and 34.62%. Present study authenticates the presence of several species of digenetic trematode parasites in the fishes inhabiting freshwater of J&K union territory.

Introduction

Fish constitutes an important source of food, nutrition, income and livelihood for millions of people around the world. Moreover, fish continues to be one of the most traded food commodities worldwide with more than half of fish exports by value originating in developing countries. Fishes provide a potential habitat to metacercariae of digenetic trematodes. Digenetic trematodes are a diverse group of parasites that use more than one host to complete their life cycle. Avian digenetic trematodes use fishes as secondary intermediate hosts to complete their life-cycles (Bullard and Overstreet 2008). Trematodes are the most diverse group of fish parasite and are present in larval or adult forms in majority of fish species and most of them exist as endoparasites. Digenetic trematode infections cause low weight gain, high mortality and immarketabilty of the infected fish. Currently, fish-borne zoonotic trematodes are the cause of health problems and also affect the public health in many Asian countries (Murrell et al. 2007; Tran et al. 2008; Phan et al. 2010). The present study was therefore undertaken to ascertain the spectrum of digenetic trematodes from fresh water fishes Ophiocephalus punctatus and Xenentodon cancila in Jammu region.

Materials And Methods

A total of 220 fish samples were collected from different freshwater bodies of Jammu region; Gho-manhasan, Chakrali and Chadwal. Collected fish samples were brought alive to laboratory. The gastrointestinal tract, muscle tissue and other internal organs of the host fish were teased in 0.8% saline and examined for the recovery of the metacercarial or adult stage oftrematode parasites. Trematode parasites were flattened between two slides or under slight pressure of slide and coverslip, post-fixed in AFA (Alcohol, Formalin and Acetic acid in 85:10:5) and stained with Borax carmine. Afterwards, specimens were dehydrated in ascending series of ethanol, cleared in xylene and finally mounted on glass slides using DPX. Photomicrographs of stained specimens were studied and photographed using microscope Leica M205 C and identified by following the standard literature (Yamaguti 1971; Bray et al. 2008; Pandey and Agrawal, 2013). The prevalence of infection and mean intensity were calculated following Bush et al. (1997).

                        No. of hosts infected 

Prevalence =  ----------------------------------- × 100 

                      Total no. of hosts examined

                              No. of parasites recovered

Mean Intensity = ----------------------------------- 

                             Total no. of infected hosts

Results & Discussion

Based on morphological and morphomertic criteria the recovered trematode parasites were identified as belonging to genera Euclinostomum (Rudoliphi, 1809) Travassos, 1928 (Family Clinostomiodae Luhe, 1901); Phyllodistomum Braun, 1899 (Family Gorgoderidae Looss, 1901); Genarchopsis Ozaki, 1925 (Family Hemiuridae (Looss, 1899, Luhe, 1901) and Bucephalopsis Diesing, 1855 (Family: Bucephalidae Poche, 1907) all of which are redescribed .

1. Euclinostomum heterostomum (Rudolphi, 1806) Travassos, 1928 (Figa)

Host: Ophiocephalus punctatus Bloch

Site of infection: Liver, Coelomic cavity, muscles

Locality: Gho-manhasan, Chakrali

Prevalence: 33.62% (39 infectedout of 116 host)

Mean intensity: 4.68 (182 parasites were recovered from 39 infected host)

Description

Cysts of E. heterostomum were yellowish and spherical, excretory vesicle, intestinal caeca brownish and are observed on the external surface; excysted metacercariae body elongated, linguiform after fixing measures 4.36-6.54mm×2.18-2.49mm; anterior end of the body truncated and posterior end is rounded; oral sucker sub-terminal, small surrounded by collar-like fold 0.19-0.38mm×0.16-0.27mm; ventral sucker lager well developed, almost round measuring 0.712-0.872mm×0.625-0.721mm; Pharynx rudimentary; oesophagus short bifurcates in front of acetabulum; intestinal caeca long with 7-12 lateral diverticulate branching; anterior testis U-shaped 0.115-0.159× 0.36-0.462mm ; posterior testis Y-shaped 0.218-0.320× 0.253-0.374mm; cirrus sac oval, intertesticular; ovary small, round to oval, intertesticular 0.121-0.146×0.140-1.28mm; uterine sac elongated and club shaped; excretory pore subterminal.

Remarks

The genus Euclinostomum was established by Travassos, 1928 which have well developed diverticulated ceaca. Moreover, Euclinostomum is the type genus of subfamily Euclinostominae, found in the buccal cavity and in the oesophagus of piscivorous birds, primarily herons and egrets. Many reports of metacercarial and adult forms of E.heterostomum from freshwater fishes have been studied by several workers across the world (Jhansilakshmibai & Madhavi 1997, Britz et al. 1984, Taher 2009, Purivirojkul and Sumontha 2012, Suanyuk et al. 2013, Senapin et al. 2014, Abro et al. 2016, Mansour 2019) from different host fishes. Present fluke exhibits similarities with E.heterostomum Rudolphi, 1809, E.bhagavantami Jaiswal, 1957, E.minutus Bhutta and Khan, 1975 and E.reticulatum Sudan, 1979 (Table no.2). In the present fluke oral sucker is subterminal closely resembles to E.reticulatum but smaller than E.bhagavantami and E.minutus. The number of intestinal diverticulae differs in E.bhagavantami (9-12), in E.minutus (12-15) whereas resembles E.reticulatum with 7-12 diverticula. The size of ovary, however show resemblance to E.minutus which is quite smaller than that of E.bhagavantami and E.reticulatum. Thus the present fluke differs from E.bhagavantami, E.minutus and E.reticulatum in body size, size of ovary and testes. The present form closely resembles Euclinostomum heterostomum in size and shape of body and various organs which is reported from host fish Ophiocephalus punctatus of Jammu region.

2. Phyllodistomum tripathi Motwani & Srivastava, 1961 (Fig.b)

Host: Xenentodon cancila Hamilton

Site of infection: Intestine

Locality: Chadwal

Prevalence: 34.62% (36 infected out of 104 host)

Mean intensity: 2.83 (102 parasites were recovered from 36 infected host)

Description

Body dorsoventrally flattened, spatulate 1.58-3.72mm long, 0.72-2.04mm maximum width at level of middle region of hindbody; fore-body narrow, elongated 0.89-0.94mm×0.43-0.75mm; hind-body expanded nearly with feebly developed semicircular puckering present on the lateral sides of hind body, 0.95-0.98mm×0.78-0.80mm in size; oral sucker terminal, oval 0.19-0.26×0.20-0.28mm; ventral sucker rounded, pre-equatorial slightly larger and wider than oral sucker 0.22-0.28mm×0.24-0.33mm;prepharynx and pharynx absent; oesophagus straight, narrow 0.12-0.17mm long bifurcates into well developed two intestinal caeca which terminate close to hind body end; testes deeply lobed, intercaecal, post-ovarian ; right testis post-equatorial 0.16-0.20×0.14-0.17mm; left testis equatorial 0.22-0.24×0.18-0.20mm; gential pore median, pre-acetabular; ovary submedian, lobed, pretesticular, 0.07-0.12mm×0.06-0.08mm; two compact vitelline glands, right vitelline gland 0.06-0.07mm×0.03-0.04mm and left vitelline gland 0.07-0.08mm×0.04-0.05mm; eggs oval, non-operculate 0.02-0.03×0.01-0.02mm.

Remarks

The genus Phyllodistomum was erected by Braun (1899) for Distomum folium Olfers, 1816 as its type species. Based on the narrow and tubular anterior region and spatulated hind body our specimen belonged to the genus Phyllodistomum. Different species of the genus Phyllodistomum have been reported by several workers (Cribb, 1987; Helt, 2003; Mendoza-Garfias et al. 2005; Ho et al. 2014) from fishes all over the world including that from India (P.loossi Kaw, 1950; P. indianum Jaiswal, 1957; P. tripathi Motwani and Srivastava, 1961; P. srivastavi Rai, 1964; P. cameroni Agarwal, 1966; P.megacotyle Fotedaar, 1969; P.mansari Sudan, 1979; P. triangulata Sarwat, 2011; P.betwaensis Sen, 2014; P.punctatai Jithila and Prasadan, 2018). The present species resembles with P.loossi in the relative size of suckers, shape and position of vitellaria, uterus and genital pore. It however differs in the absence of any papillae in suckers and the size of eggs which are smaller and more slender in present form. The present species shows similarities with P.betwaensis but different from P.betwaensis in size of body, size of oral and ventral sucker and position of Vitelline glands with respect to ovary (Table no. 3). The present species differ further from P.punctati, a species reported from urinary bladder of Channa punctata in ratio of body length to width, size of oral and ventral sucker and various morphological and morphometry features. Present species resembles P.tripathi in having the lateral margins of hindbody provided with indentations, however differs in some morphological features and morphometry like length to width ratio of body, size and shape of ventral sucker and size of testes and ovary. Since, most of the characteristics of the present species bear a close resemblance with P.tripathi hence the identified as P.tripathi reported from freshwater fish Xenentodon cancilla of Jammu.

3. Genarchopsis piscicola Srivastava, 1933 (Fig.c)

Host: Xenentodon cancilla Hamilton

Site of infection: Stomach

Locality: Chakrali, Chadwal

Prevalence: 40.38% (42 infected out of 104 host)

Mean intensity: 2.95 (124 parasites were recovered from 42 infected host)

Description

Body cylindrical, more or less fusiform, 1.28-2.57×0.42-0.79mm; oral sucker oval, sub-terminal 0.24-0.38×0.26-0.47mm; ventral sucker equatorial, highly muscular and well developed 0.56-0.79×0.58-0.80mm; prepharynx absent; pharynx 0.03-0.07×0.09-0.12mm; oesophagus absent; testes two, roughly triangular or oval in outline, extracaecal; right testis 0.16-0.17×0.12-0.14mm; left testis 0.15-0.17×0.13-0.14mm; pars-prostatica tubular and well developed; metraterm absent; genital pore present below pharynx near intestinal bifurcation; ovary 0.13-0.18×0.09-0.15mm posttesticular, oval, median or dextrally placed between testes and vitelline glands two, oval, compact 0.15-0.20×0.08-0.012mm; eggs oval, operculated bear long filaments 0.032-0.035×0.009-0.016mm.

Remarks

The genus Genarchopsis was erected by Ozaki (1925) with G. goppo as the type species from the intestine of Mogurnda obscura, Japan. Several species of Genarchopsis have been reported viz. G. ovocaudata Srivastava, 1933 from Ophiocephalus punctatus; G. piscicola Srivastava, 1933 from Channa punctatus; G. anguillae Yamaguti, 1938 from Anguilla japonica G. folliculate Bhadauria and Dandotia, 1954 from Mastacembelus sp. and Channa sp.; G. thapari Dwivedi, 1965 from Bufo melanostictus; G.punctati Agarwal, 1966 from Ophiocephalus punctatus; G. cameroi Kakaji, 1969 from Mystus seenghala; G. cuchiai Kakaji, 1969 from Amphipnous cuchia; G. avitellarium Varma and Sahay, 1983 from Ophiocephalus punctatus; G. kalriai Bilqees and Khan, 1990 from Channa marulius; G.fellicola Shimazu, 1995 from Rhinogobius brunneus; G.gibsoni Shaikh et al., 2011 from Opiocephalus striatus. The present parasite resembles closely with G. piscicola, G.goppo and G.gibsoni (Table no. 4). The present form differ markedly from Ozaki’s species G.goppo in larger body size, size and ratio of suckers, position of genital pore, absence of oesophageal pouch, location of gonads, position of vitellaria and position of ventral sucker. It differs from G.gibsoni in various morphological features and morphometry in body size, size of oral and ventral sucker, position and shape of testes and ovary. But the present form shows comes very close to G.piscicola in position of oral sucker, size and ratio of suckers, absence of oesophagus, shape and disposition of testes and position of gential pore. The present species is redescribed as G.piscicola and reported from different host Xenentodon cancila of Jammu region.

4. Bucephalopsis karvei Bhalerao, 1937 (Fig.d)

Host: Xenentodon cancila Hamilton

Site of infection: Intestine

Locality: Chadwal

Prevalence: 26.93% (28 infected out of 104 host)

Mean intensity: 3.92 (110 parasites were recovered from 28 infected host)

Description

Body small pear-shaped with broader anterior end and a pointed posterior end measuring 0.57-0.98mm×0.31-0.52mm; tegument covered with spines; rhynchus (anterior sucker) large, spherical, terminal, 0.11-0.23mm×0.13-0.20mm; pharynx muscular, oval 0.05-0.06mm×0.04-0.07mm;esophagus tubular opens into digestive cecum; cecum globular sac-like, median 0.06-0.09mm×0.06-0.01mm; testis oval, unequal, anterior testis 0.12-0.14mm×0.08-0.09mm, posterior testis 0.11-0.13mm×0.07-0.09mm; cirrus sac cylindrical, extent from level of testis to posterior of body 0.24-0.28mm×0.05-0.07mm; pars prostatica opens into short ejaculatory duct; ovary oval, pre-testicular, 0.06-0.08×0.07-0.09mm; egg numerous oval, 0.017-0.018×0.009-0.012mm.

Remarks

Diesing (1855) erected Bucephalopsis as subgenus of Bucephalus Von Baer, 1827 for Bucephalus hairreanus Lacaze-Duthiers, 1834 and was later raised to full generic status by Laebour (1908). Srivastava and Chauhan (1973) treated Bucephaloidea as a junior synonym of Prosorhynchoides and transferred Bucephaloides sp. to the Genus Prosorynchoides based on the presence of simple sucker (rhynchus) and a pretesticular ovary in it. Several species of Genus Bucehalopsis (Prosorynchoides) have been reported from India; these include P.fusiformis (Verma, 1936) Srivastava and Chauhan 1973; P.garuai Verma, 1936; P.magnum Verma, 1936; P.karvei (Bhalerao, 1937) Srivastava and Chauhan 1973; P.thapari (Dayal, 1948) Bott and Cribb, 2005. Maurya et .al., (2018) synonymized P.lateroporus, P.gaurii, P.chauhani, N.(P.) jhansiansis and P.canciliansis with P.karvei. The present form belongs to the genus Bucephalopsis Diesing, 1855. Bhalerao (1937) reported B. karvei from the intestine of Xenentodon cancila. The present adult worms were also recovered in large number from the intestine of Xenentodon cancila and closely resemble B.karvei in body shape, position of testes and ovary, but differ in some morphological and morphometric characters. The present adult worms differs from P.garuai, P.fusiformis and B. thapari in various morphological and morphomertic characters size and shape of body, size of rhynchus, position of ovary and testes and also size and disposition of cirrus sac and uterus (Table no.5). This bucephalid is new locality record observed for the first time in Jammu region, J&K.

Declarations

Conflict of interest: The authors declare that there is no conflict of interest.

Ethical approval: No approval by an ethical committee was required to achieve the goals of the present study.

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Tables

Table 1: Digenetic trematodes recovered, their host, site of collection and prevalence of infection from Jammu region. 

Table 2: Comparative measurements of Euclinostomum heterostomum with other species of Euclinostomum (in mm).

Table 3: Comparative measurements of Phyllodistomum tripathi with other species of Phyllodistomum (in mm).  

Table 4: Comparative measurements of Genarchopsis pisicola with other species of Genarchopsis. 

 Table 5: Comparative measurements of Bucephalopsis (Prosorhynchoides) karvei with other species of Bucephalopsis (Prosorhynchoides) (in mm)