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. 2018 Mar 22;42(2):226–231. doi: 10.1007/s12639-018-0988-9

Description of Tetracotyle wayanadensis n. sp. (Digenea: Strigeidae) metacercaria infecting six species of freshwater fishes from Western Ghats, India

P J Jithila 1, P K Prasadan 1,✉
PMCID: PMC5962497  PMID: 29844627

Abstract

Tetracotyle wayanadensis n. sp. (Digenea, Strigeidae) infecting different organs of six species of freshwater fishes, Haludaria fasciata (eye, buccal cavity), Amblypharyngodon melettinus (eye, buccal cavity), Aplochelus lineatus (operculum, heart, mesenteries), Pethia conchonius (brain), Parambassis thomassi (muscles, mesenteries) and Lepidocephalus thermali (mesenteries) collected from water bodies in the Wayanad region of the Western Ghats is described and illustrated. Tetracotyle wayanadensis n. sp. is new to the genus and is separated from its congeners on the basis of differences in morphology and morphometry. The present paper also describes the prevalence, intensity, mean abundance and sites of infection of the parasite in each host. The prevalence of infection of T. wayanadensis n. sp. in Haludaria fasciata is 7.5%, intensity of infection is 2.66 and mean abundance is 0.2; in Amblypharyngodon melettinus 10%, 6 and 0.6; in Aplochelus lineatus 12.2%, 6.2 and 0.76; in Pethia conchonius 7.14%, 5 and 0.36; in Parambassis thomassi 100%, 2 and 2; in Lepidocephalus thermali 10%, 2 and 0.2 respectively.

Keywords: Tetracotyle wayanadensis, Digenetic, Trematode, Freshwater fish, Prevalence, Intensity, Western Ghats

Introduction

Western Ghats is rich in freshwater fish diversity and endemism. Dhanukar et al. (2011) reported that 290 species of freshwater fishes belonging to 11 orders, 33 families and 106 genera were documented from the Western Ghats region, of which 189 species (65%) are endemic. Freshwater fishes act as potential hosts for adults as well as larval stages of digenetic trematodes. Hughes (1928), Stunkard (1973), Cone and Anders (1977), Barson et al. (2008) and Gholami et al. (2011) studied Tetracotyle infection in freshwater fishes. Literature survey revealed that there are several studies on the genus Tetracotyle infecting freshwater fishes of India, which included that of Singh (1956), Rai and Pande (1969), Chakrabarti (1970a, b), Chakrabarti and Baugh (1970), Pandey (1971), Baugh and Chakrabarti (1977), Agarwal and Khan (1982), Pandey and Tiwari (1983), Tewari and Tyagi (1986), Pandey and Pandey (2000), Sheena and Janardanan (2008) and Vankara et al. (2011). According to Pandey and Agarwal (2013) 29 species of this genus have been described from freshwater fishes of India. Shini et al. (2015) reported a species of Tetracotyle infecting cyprinid fish, Devario malabaricus (Jerdon) from Kerala. Gupta (2016) reported two new species of Tetracotyle (Tetracotyle bhopalensis and Tetracotyle mauensis) from Indian freshwater food fishes.

The paper describes the morphological features and taxonomic status of a new species of digenetic trematode metacercaria, Tetracotyle wayanadensis n. sp. infecting brain, heart, eyes, buccal cavity, operculum, muscles and mesenteries of freshwater fishes collected from different water bodies in the Wayanad region of the Western Ghats. It also describes the prevalence, intensity, mean abundance and sites of infection of the parasite in each host and discussed.

Materials and methods

Study area

The study was carried out in the Wayanad region of the Western Ghats. Western Ghats of India is considered as one of the 34 global biodiversity hotspots owing to its rich biodiversity and endemism. The map of the study area (Fig. 1) was prepared using QGIS 2.16.1 software.

Fig. 1.

Fig. 1

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Study area—Western Ghats—Wayanad region

Methods

Host specimens were collected from hill streams, small rivulets and ponds in different localities, using sweep net. The collected fishes were brought alive to the laboratory in suitable containers and maintained in clean, aerated glass tanks or aquariums. Fishes were fed occasionally with cooked rice, fish meal or biscuit crumbs. Fishes were sacrificed by cervical rupture and their scales, skin, gills, gill chambers and eyes were examined under a Labomed (Luxeo 4Z) stereozoom microscope for larval digeneans. Skin was removed, and muscle tissues were macerated to detect the metacercariae, if any. Internal organs like heart, liver, gall bladder, pancreas, intestine, kidney, urinary bladder, swim bladder, gonads and brain were dissected out, placed in separate petri dishes containing 0.75% saline, macerated and examined under the stereozoom microscope. Metacercariae, when present, were carefully transferred to 0.75% saline in a petri dish. Metacercarial cysts were mounted on a slide with saline and examined under a Nikon ECLIPSE Ni-U phase contrast research microscope (Nikon, Japan) for detailed study. Larvae were excysted either by rupturing the cyst wall with fine needles or by mounting them under cover glass and applying gentle pressure using fine needles. The excysted larvae were studied under the phase contrast microscope without vital staining or with neutral red or methylene blue stains. Permanent whole mounts of excysted larvae were prepared by fixing them in 5% formalin under slight cover glass pressure, and staining with acetocarmine, following the procedure outlined by Cantwell (1981). Photographs were taken with Nikon Y-TV55 camera and Nikon NIS Elements imaging software. Figures were drawn with Nikon Y-IDT drawing tube and measurements (in µm) were taken with Nikon NIS Elements imaging software.

Results

Tetracotyle wayanadensis n. sp. (Fig. 2)

Fig. 2.

Fig. 2

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Tetracotyle wayanadensis n. sp., metacercaria

Cyst oval, single-layered, thin, transparent, devoid of pigments. Body aspinose, broadly oval, divided into fore- and hind-bodies. Fore-body large, measured 687.10–987.24 × 670.20–902.71 (793.11 × 755.72) and hind body measured 186.95–405.62 × 236.22–407.78 (258.60 × 301.95); length to width ratio of body is 1.38:1. Oral sucker terminal, round to ovoid, 67.55–104.82 × 55.18–184.48 (82.66 × 100.41). Ventral sucker ovoid, pre-equatorial in the forebody 84.17–128.36 × 105.45–133.54 (111.12 × 119.90). Two prominent accessory suckers, one on either side of oral sucker, 212.43–337.94 × 100.73–171.79 (280.39 × 135.01). Hold fast organ 168.00–295.48 × 324.55–445.98 (240.89 × 396.47), close to ventral sucker. Hold fast gland absent or not discernible. Prepharynx absent. Pharynx, round to oval, 26.55–48.01 × 22.17–43.18 (39.43 × 31.37) leading to esophagus 107.14–171.60 (147.32). Intestinal caeca 552.79–967.42 (723.34) extending up to posterior end of the body, width increases posterior to holdfast organ. Gonads represented by two oval, tandem masses, posterior to hold fast organ 20.00–50.17 × 41.44–143.48 (35.93 × 96.05). Excretory bladder at posterior end of body, 73.36–81.14 × 48.03–61.34 (74.75 × 54.33); excretory pore terminal.

Taxonomic summary

Type specimen: Holotype (No. Z-P/H-F 75) deposited in the Helminth parasite collections, Ecological Parasitology and Tropical Biodiversity Laboratory, Department of Zoology, Kannur University, Mananthavady Campus, Wayanad-670645, Kerala, India.

Type hosts: Haludaria fasciata (Z-FF-5), Amblypharyngodon melettinus (Z-FF-4), Aplochelus lineatus (Z-FF-8), Pethia conchonius (Z-FF-11), Parambassis thomassi (Z-FF-9) and Lepidocephalus thermali (Z-FF-7). Deposited in the Ichthyology collections, Department of Zoology, Kannur University, Mananthavady Campus, Wayanad-670645, Kerala, India.

Type localities: Thrisileri, Pakkam, Panamaram, Neervaram, Karakuni, Kakkancheri, Vellamunda and Chooralmala, Wayanad, Kerala, India.

Period of collection: April 2017 to November 2017.

Prevalence, intensity, mean abundance and the sites of infection (Table 2) vary with host species. Prevalence of infection and mean abundance appeared higher in Parambassis thomassi, whereas intensity was higher in Aplochelus lineatus among the host fishes studied.

Table 2.

Prevalence, intensity, mean abundance and site of infection in fish hosts

Host Prevalence of infection (%) Intensity of infection Mean abundance Site of infection
Haludaria fasciata 6/80 (7.50) 2.66 0.2 Eye, buccal cavity
Amblypharyngodon melettinus 1/10 (10) 6 0.6 Eye, buccal cavity
Aplochelus lineatus 5/41 (12.20) 6.20 0.76 Operculum, heart, mesenteries
Pethia conchonius 1/14 (7.14) 5 0.36 Brain
Parambassis thomassi 2/2 (100) 2 2 Muscles, mesenteries
Lepidocephalus thermali 1/10 (10) 2 0.2 Mesenteries
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Discussion

The genus Tetracotyle was established by De Filippi in 1854. Hoffman (1960) described the salient features of Tetracotyle De Fillipi, 1854. Tetracotyle spp. mainly parasitizes intestine, mesenteries, muscles, liver, ovary, cranial cavity, pericardium, gills, subcutaneous tissue and fin of freshwater fishes. Ashworth and Bannerman (1927) reported Tetracotyle phoxini in the brain of a freshwater fish. Vankara and Chikkam (2013) studied Tetracotyle infecting heart tissue of the freshwater fish, Mastacembelus armatus.

Thirty two species of Tetracotyle have been described from freshwater fishes of India so far. T. sophoriensis (Singh, 1956), T. indicus (Singh, 1956), T. ujjainensis (Trivedi, 1964), T. mesentriformis (Rai and Pande, 1964), T. gorakhpurensis (Rai and Pande, 1969), T. fausti (Rai and Pande, 1969), T. mathuraensis (Rai and Pande, 1969), T. szidati (Chakrabarti and Baugh, 1970), T. xenentodoni (Chakrabarti, 1970a), T. muscularis (Chakrabarti, 1970b), T. glossogobii (Chakrabarti, 1970c), T. lali (Pandey, 1970), T. lucknowensis (Pandey, 1971), T. singhi (Pandey, 1973), T. baughi (Pandey, 1973), T. tandoni (Pandey, 1973), T. aglandulata (Baugh and Chakrabarti, 1977), T. gyanpurensis (Agarwal and Singh, 1980), T. pandei (Agarwal and Khan, 1982), T. srivastavai (Agarwal and Khan, 1982), T. ramalingi (Agarwal and Khan, 1982), T. simhai (Pandey and Tiwari, 1983), T. sanjivi (Pandey and Tiwari, 1983), T. fotedari (Pandey and Tiwari, 1983), T. satendri (Tewari and Tyagi 1986), T. kalyani (Pandey and Pandey, 2000), T. satyapali (Pandey and Pandey, 2000), T. janardani (Sheena and Janardanan, 2008), Tetracotyle sp. 1 (Vankara et al. 2011), Tetracotyle sp. (Shini et al. 2015), Tetracotyle bhopalensis (Gupta, 2016) and Tetracotyle mauensis (Gupta, 2016).

The present species exhibits similarities with T. tandoni, T. lucknowensis and Tetracotyle sp. (Table 1). It differs from T. tandoni in various morphological features and morphometry like presence of cyst, length to width ratio of body, size and shape of oral sucker, size of ventral sucker, absence of hold fast gland, length of ceacae and position of gonads.

Table 1.

Comparison of morphologic and morphometric characters of T. tandoni, T. lucknowensis, Tetracotyle sp. and T. wayanadensis n. sp

Characters T. tandoni (Pandey, 1973) T. lucknowensis (Pandey, 1971) Tetracotyle sp. (Shini et al., 2015) T. wayanadensis n. sp.
Cyst No cyst Oval, thin, transparent, devoid of pigments Oval, milky white, double layered cyst wall Oval, thin, transparent, devoid of pigments; single layered cyst wall
Body L × B Aspinose, with fore and hind body 610–710 × 410–50 (660 × 430) Aspinose, broadly oval, fore and hind body not clearly marked 480–670 × 360–480 (575 × 420) Aspinose, oval, divided into large fore-body, 402.5–1015 × 315–857.5 (708.75 × 586.25) and small hind-body 70–350 × 175–332.5 (210 × 253.75) Aspinose, divided into fore-body 687.10–987.24 × 670.20–902.71 (793.11 × 755.72) and hind body 186.95–405.62 × 236.22–407.78 (258.60 × 301.95), length to width ratio is 1.38:1
Oral sucker L × B Round 60–70 Sub terminal 70–90 Terminal, round to oval, 35–70 × 52.5–87.5 (52.5 × 70) Terminal, round to oval, 67.55–104.82 × 55.18–184.48 (82.66 × 100.41)
Ventral sucker L × B 50–190 Pre-equatorial, 90–120 × 80–90 (105 × 85) Oval 87.5–105 × 105–122.5 (96.25 × 113.75) Oval, pre-equatorial larger than oral sucker 84.17–128.36 × 105.45–133.54 (111.12 × 119.90)
Accessory suckers L × B Psuedo suckers in the anterior region of the body Large, prominent, covering almost entire lateral region of the body Prominent, two, - one on either side of oral sucker 70–192.50 × 35–70 (131.25 × 52.50) Two, prominent, one on either side of oral sucker, 212.43–337.94 × 100.73–171.79 (280.39 × 135.01)
Holdfast organ L × B Large, bilobed, holdfast gland present Close to VS, Holdfast gland absent Well developed, behind VS 140–315 × 52.5–140 (227.5 × 96.25). Holdfast gland large 385–717.5 × 35–105 (551 × 70) Close to VS 168.00–295.48 × 324.55–445.98 (240.89 × 396.47). Holdfast gland absent
Pharynx L × B Pharynx 20–30 – Small, globular, measured 17.5–40 × 17.5–37.5 (28.75 × 27.5) Round to oval 26.55–48.01 × 22.17–43.18 (39.43 × 31.37)
Ceaca L × B Extending up to hind body Extending up to hind region of the body Extending up to the posterior third of body Extending up to posterior end of the body 552.79–967.42 (723.34); width increases posterior to holdfast organ
Gonads L × B Two, large oval masses, one behind other representing testes. Oval ovarian rudiment, level with anterior testes Two, oval, post-acetabular masses Reproductive organs rudimentary; posterior part of hind body Two, oval, tandem masses, posterior to hold fast organ 20.00–50.17 × 41.44–143.48 (35.93 × 96.05)
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The present species deserves comparison (Table 1) with T. lucknowensis also. In spite of the similarities, it differs from T. lucknowensis in many morphological features and morphometry including the ratio of body length to width, size and shape of oral sucker, size of ventral sucker, and position & nature of gonads.

The present species shows some similarities with Tetracotyle sp. Shini et al. 2015 too. It differs from Tetracotyle sp. in many morphological features and morphometry like the number of layers on the cyst wall, size of body, oral sucker, accessory suckers, and holdfast organ, absence of holdfast gland, shape and size of pharynx and length of ceacae.

Apart from the above, the hosts of the present species are different and are from different geographical region. Moreover, the present species has been recovered from six species of fishes; Haludaria fasciata, Amblypharyngodon melettinus, Aplochelus lineatus, Pethia conchonius, Parambassis thomassi and Lepidocephalus thermali.

Parasites often exploit more than one host species at any given stage in their life cycle (Poulin 1992). In the present study six fish species serve as hosts and the parasites are unevenly distributed in different organs of these hosts. The ability to exploit many host species is often associated with a lower average efficiency of host exploitation (Poulin 2005). According to Galaktionov and Dobrovolskij (2003) the metacercaria larvae settle in different biotopes in the host body. They also pointed out that the strigeidids parasitizing fish can use almost all tissues/organs of the host fish possible. The present study agrees with Galaktionov and Dobrovolskij (2003).

The result may also indicate that the ecological similarity among host species was a reason for the parasite to choose more than one host. From an ecological perspective, some host species are parasitised more intensely than others. That is, the prevalence, intensity, or abundance of infection by a particular parasite differs among its host species (Poulin and Mouillot 2005). In the present study prevalence, intensity and abundance of infection varied with host species and, therefore, is in agreement with the findings of Poulin and Mouillot (2005). Variation in infection levels, such as prevalence, intensity and abundance, by a parasite among its different host species may also reflect parasite specialization (Poulin 2005).

Acknowledgements

The authors are grateful to the Kerala State Council for Science, Technology and Environment (KSCSTE), Government of Kerala for providing infrastructure facilities in the laboratory through a major research project (SRS/220/2015/KSCSTE). The authors are indebted to Prof. K. P. Janardanan for critically going through the manuscript.

Author’s contribution

Dr. P. K. Prasadan designed and guided the study. Ms. Jithila P J. carried out the survey, collected and studied the trematodes in detail. The manuscript was written by both the authors.

Compliance with ethical standards

Conflict of interest

The authors declare that that there is no conflict of interest between them.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in the study involving animals were in accordance with the ethical standards of the institution or practice at which the study was conducted.

References

  1. Agarwal N, Khan S. Studies on some Tetracotyle Fillipi (1982) metacercariae from fishes of Lucknow. Proc Indian Acad Sci. 1982;91:515–522. doi: 10.1007/BF03186151. [DOI] [Google Scholar]
  2. Agarwal N, Singh HS. Infection of Channa punctatus (Bloch) with a metacercaria Tetracotyle gynapurensis n. sp. Matsya. 1980;6:84–86. [Google Scholar]
  3. Ashworth JH, Bannerman JCW. On a Tetracotyle (T. phoxini) in the brain of the Minnow—VIII. Trans R Soc Edinb. 1927;55(1):159–172. doi: 10.1017/S008045680001629X. [DOI] [Google Scholar]
  4. Barson M, Bray R, Ollevier F, Huyse T. Taxonomy and faunistics of the helminth parasites of Clarias gariepinus (Burchell, 1822), and Oreochromis mossambicus (Peters, 1852) from temporary pans and pools in the Save-Runde river floodplain, Zimbabwe. Comp Parasitol. 2008;75(2):228–240. doi: 10.1654/4337.1. [DOI] [Google Scholar]
  5. Baugh SC, Chakrabarti KK. On a triple infection of strigeid metacercaria in an Indian freshwater fish Xenentodon cancila. Parasitol. 1977;18:84–94. [PubMed] [Google Scholar]
  6. Cantwell GE. Methods for invertebrates. In: Clark G, editor. Staining procedures. Baltimore: Williams and Wilkins; 1981. pp. 255–280. [Google Scholar]
  7. Chakrabarti KK. Two new species of strigeid metacercariae from an Indian freshwater fish, Xenentodon cancila (Ham.) Proc Helminth Soc Wash. 1970;37:5–10. [Google Scholar]
  8. Chakrabarti KK. A double metacercarial infection in an Indian freshwater fish, Heteropneustes fossilis (Bloch) Rev Biol Trop. 1970;17(1):91–96. [Google Scholar]
  9. Chakrabarti KK. A new strigeid metacercaria, Tetracotyle glossogobii n. sp., from Indian freshwater fish, Glossogobius giuris (Ham.) Helminthologia. 1970;11:1–4. [Google Scholar]
  10. Chakrabarti KK, Baugh SC. Tetracotyle Szidati n. sp. A metacercaria from the Indian freshwater fish, Channa punctatus (Bloch) Indian J Zoot. 1970;11:79–82. [Google Scholar]
  11. Cone DK, Anders RC. Parasites of pumpkin seed (Lepomis gibbosus L.) from Ryan Lake, Algonquin Park, Ontario. Can J Zool. 1977;55:1410–1423. doi: 10.1139/z77-184. [DOI] [PubMed] [Google Scholar]
  12. Dhanukar N, Raghavan R, Ali A, Abraham R, Shaji C (2011) The status and distribution of freshwater fishes of the Western Ghats. In: Molur S, Smith KG, Daniel BA, Darwall WRT (eds) International Union for Conservation of Nature (IUCN) Gland, Switzerland and Zoo Outreach Organization (ZOO), Coimbatore, pp 21–48
  13. Galaktionov KV, Dobrovolskij AA. The biology and evolution of trematodes. Dordrechet: Springer; 2003. pp. 304–310. [Google Scholar]
  14. Gholami Z, Akhlaghi M, Mobedi I, Esmaeili HR. Infection of Aphanius sophiae (Actinoptrygii: Cyprinodontidae) with Tetracotyle sp. Vet Res Forum. 2011;2(1):65–68. [Google Scholar]
  15. Gupta BK. Studies on the structure of three new species of Strigeids metacercariae from Indian freshwater food fishes. Int J Pure Appl Biosci. 2016;4(4):221–228. doi: 10.18782/2320-7051.2347. [DOI] [Google Scholar]
  16. Hoffman GL. synopsis of strigeoidea (trematoda) of fishes and their life cycles. Washington: U.S. Fish and Wildlife Service; 1960. pp. 439–466. [Google Scholar]
  17. Hughes RC. Studies on the trematode family Strigeidae (Holostomidae) No. XIII. Three new species of Tetracotyle. Trans Am Microsc Soc. 1928;47(4):414–433. doi: 10.2307/3222239. [DOI] [Google Scholar]
  18. Pandey KC. Studies on metacercaria of freshwater fishes of India. III On two new species of Diplostomulum Brandes, 1982. Proc Indian Acad Sci. 1970;42:162–170. [Google Scholar]
  19. Pandey KC. Studies on metacercaria of freshwater fishes of India. VIII On the morphology of Tetracotyle lucknowensis n. sp. from Channa punctatus (Bloch) Proc Indian Acad Sci. 1971;44:1–5. [Google Scholar]
  20. Pandey KC. Studies on metacercaria of freshwater fishes of India. II Description of a known and five unknown strigeid metacercariae from Lucknow. Indian J Zoot. 1973;14:155–166. [Google Scholar]
  21. Pandey KC, Agarwal N. Metacercarial fauna of India. Kolkata: Zoological Survey of India; 2013. pp. 9–45. [Google Scholar]
  22. Pandey KC, Pandey N. Studies on two new stigeid metacercariae from Xenetodon cancila (Ham.) Indian J Helminth. 2000;17:29–32. [Google Scholar]
  23. Pandey KC, Tiwari SK. Studies on some new strigeid metacercariae. J Adv Zool. 1983;4:115–122. [Google Scholar]
  24. Poulin R. Determinants of host specificity in parasites of freshwater fishes. Int J Parasitol. 1992;22:753–758. doi: 10.1016/0020-7519(92)90124-4. [DOI] [PubMed] [Google Scholar]
  25. Poulin R. Relative infection levels and taxonomic distancesamong the host species used by a parasite: insights into parasite specialization. Parasitology. 2005;130:109–115. doi: 10.1017/S0031182004006304. [DOI] [PubMed] [Google Scholar]
  26. Poulin R, Mouillot D. Host specificity and the probability of discovering species of helminth parasites. Parasitology. 2005;130:709–715. doi: 10.1017/S0031182004007218. [DOI] [PubMed] [Google Scholar]
  27. Rai P, Pande BP. On the metacercarial fauna of the Indian fresh water scombresocid fish Belon cancila. Indian J Fish. 1964;11:315–320. [Google Scholar]
  28. Rai P, Pande BP. On the morphology and pathogenic significance of the strigeoid metacercariae in some Indian freshwater fishes. I. Tetracotyle and Neascus. Indian J Anim Sci. 1969;39:355–359. [Google Scholar]
  29. Sheena P, Janardanan KP. Six species of metacercaria (Digenea: Trematoda) from Etroplus maculates (Bloch) in the Chaliyar river of Kerala, India. Uttar Pradesh J Zool. 2008;28:43–49. [Google Scholar]
  30. Shini KK, Preethakumari VM, Ramitha UC, Vasandakumar MV. Helminth parasitic fauna of a cyprinid fish Devario malabaricus (Jerdon) Int J Fish Aquat Stud. 2015;2(5):175–179. [Google Scholar]
  31. Singh RN. Studies on a new strigeoid metacercaria parasitic in cyprinoid fishes. Proc Nat Acad Sci. 1956;26:255–263. [Google Scholar]
  32. Stunkard HW. Studies on larvae of Strigeoid trematodes from the Woods Hole, Massachusetts Region. Biol Bull. 1973;144(3):525–540. doi: 10.2307/1540306. [DOI] [Google Scholar]
  33. Tewari SK, Tyagi V. A new Tetracotyle larva T. satendri n. sp. from Channa punctatus (Bloch) Indian J Helminth. 1986;3:91–95. [Google Scholar]
  34. Trivedi HS. On two metacercaria from freshwater fishes in Ujjain. J Vik Univ. 1964;8:91–94. [Google Scholar]
  35. Vankara AP, Chikkam V. Histopathology of heart of freshwater spiny eel, Mastacembelus armatus naturally infected with Tetracotyle metacercaria (Trematoda: Strigeidae) Res J Parasitol. 2013;8(2):45–54. doi: 10.3923/jp.2013.45.54. [DOI] [Google Scholar]
  36. Vankara AP, Mani G, Vijayalakshmi C. A report on various digenetic metacercariae from the freshwater fishes of River Godavari, Rajahmundry. J Parasit Dis. 2011;35(2):177–185. doi: 10.1007/s12639-011-0041-8. [DOI] [PMC free article] [PubMed] [Google Scholar]

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