Bulletin of Pure and Applied Sciences Print version ISSN 0970 0765 Vol.40A (Zoology), No.1, Online version ISSN 2320 3188 January-June 2021: P.176-191 DOI 10.5958/2320-3188.2021.00021.8

Content Available online at: https://www.bpasjournals.com/zoology

Review Article

Biodiversity of Parasitic Trematode sp. Looss, 1894 (: Allocreadiidae): A Review

1Sushil Kumar Upadhyay*, 2Babita

ABSTRACT: Author’s Affiliation: Although there are many heartening studies 1,2Department of Biotechnology, have been done on the parasitic helminthes of Maharishi Markandeshwar (Deemed to vertebrates but there are serious deficiencies in be University) Mullana-Ambala, checklist of trematodes Allocreadium Looss Haryana- 133207, India (Digenea: Allocreadiidae). The present study based on the literature survey to tabulate *Corresponding author: biodiversity of Allocreadium Looss reported from various hosts in the India and worldwide so far. Dr. Sushil Kumar Upadhyay, Allocreadium sp. is one of the most important Assistant Professor, parasitic digenean trematode with wide Department of Biotechnology, geographic distribution range across the world. Maharishi Markandeshwar (Deemed to The findings reflected that these trematodes be University), Mullana-Ambala (HR)- infecting very wide range of hosts from 133207, India invertebrates to vertebrates. About 104 E-mail: [email protected] Allocreadium sp. have been summarized in ORCID: https://orcid.org/0000-0002- present review recovered from various hosts 1229-4275 including 44 Indian species as well. As the aquaculture playing a key role in the food security and economy of country that is Article Info: deteriorating due to heavy parasitic load in Received on 16.02.2021 fishes. Therefore, awareness, knowledge of Accepted on 17.05.2021 biodiversity and causes of parasites should be in Published on 15.06.2021 the society at grassroots level. The authors wish to suppose that current review might be helpful in the strategic management of aquaculture for health, economy and sustainable development.

Keywords: Trematode, Helminthes, Parasite, Allocreadium sp., Host, Fish, Digenea, Aquaculture, Biodiversity, Disease.

INTRODUCTION Farzana et al., 2019). The marine and fresh water faunal resources are The two third part of the globe is covered contributing immensely in food security by water bodies (Mackenzie, 2011). The and economy worldwide (Vörösmarty et India is surrounded by aquatic system al., 2000; Mackenzie, 2011; Jaiswal et al., surrounded by three directions and 2013; Ringler et al., 2016). The fresh comprising prosperous network of fresh water and marine system are water bodies like rivers and their more common shelter for various species tributaries as well (Upadhyay, 2012; of parasitic helminthes (Malhotra et al.,

How to cite this article: Upadhyay, SK. and Babita (2021). Biodiversity of Parasitic Trematode Allocreadium sp. Looss, 1894 (Digenea: Allocreadiidae): A Review. Bulletin of Pure and Applied Sciences-Zoology,40A(1), 176-191.

Biodiversity of Parasitic Trematode Allocreadium sp. Looss, 1894 (Digenea: Allocreadiidae): A Review

2009; Kumar et al., 2011; Upadhyay et production (Shoop, 1988; Upadhyay and al., 2013a; Kumari and Perveen, 2017). Singh, 2018; Upadhyay et al., 2019b; Fishes carry parasitic helminthes infra Upadhyay et al., 2019c; Upadhyay et al., community as biological tags and serve as 2020). Allocreadium sp. (Looss, 1894) is the potent source of these parasites for the parasitic trematodes and most autogenic and others infection either commonly found in fresh water cat fishes utilizing same habitat or different and cyprinid fish. This is widely ecosystem (Shoop, 1988; Upadhyay et al., distributed in Asia continent (Looss, 2009; Jaiswal et al., 2014a). The 1900). Allocreadium sp. belongs to the digeneans are important group of family Allocreadiidae Stossich, 1904 and helminth parasites, usually invade gastro- intestinal parasite microfauna all over the intestinal tract of fresh water as well as world. It is recorded from Asia (India), marine Piscean hosts (Upadhyay et al., Nagano (Central Japan), United States of 2013b; Jaiswal et al., 2014b; Upadhyay Russia, Alahama and Florida, Argentina, et al., 2015a; Upadhyay et al., 2015b; Poland and China (Hasegawa and Ozaki Selbach et al., 2020). Fishes are 1926; Koval, 1950; Thomas, 1957; Rai, important due to its high nutritional, 1962; Roytman, 1963; Grabda, 1971; medicinal and economic values, therefore Yamaguti, 1971; Wierzbicka, 1977; Ernest known to be the Gold coin of aquatics et al., 1993; Shimazu et al., 2000; (Kumar and Upadhyay, 2016; Upadhyay, Shimazu, 2003; Gao et al., 2008; 2016a; Upadhyay, 2016b; Babita et al., Shimazu et al., 2011; Chandra et al., 2019; Nanware et al., 2019; Wake and 2019). The fishes are used as hosts by Geleto 2019). Majority of fresh water helminth parasites for food, shelter, affect fishes carry heavy infection of digenean internal organs and also alter parasites which cause deterioration in the morphological characters (Upadhyay, food value of fish and may even result in 2012; Shimazu et al., 2016; Chandra et their mortality (Upadhyay, 2012; al., 2019; Upadhyay et al., 2020; Upadhyay, 2016c; Upadhyay et al., 2016; Kashinskaya et al., 2021; Montes et al., Rani et al., 2019). Besides these, there are 2021). The present communication deals a number of helminth parasites, which with worldwide distribution of are transmitted to human beings only Allocreadium species so far. through fishes due to weak association of host and parasites called zoonotic BIODIVERSITY OF ALLOCREADIUM parasites that may affect the general LOOSS IN INDIA public health (Youn, 2009; Singh et al., 2010; Miranda, 2018; Upadhyay, 2020a; Genus Allocreadium was discovered by Upadhyay, 2020b; Upadhyay, 2020c; Looss in 19th century for the first time Upadhyay and Nanware, 2020; Majewska and named as A. isoporum Looss (1894; et al., 2021; Santan-Lima et al., 2021). 1900; 1902) that was later recovered These parasites use the fish for their redescribed as A. annandelei from shelter, food and destruct more or less Rhynchobatus djiddensis each and every organ resulting by in Southwell and Prasad (1913). deformities in external as well as internal Thereafter, Thaper and Dayal reported morphological changes (Roberts and Allocreadium sp. from Leuciscus indicus in Janovy, 2009; Upadhyay, 2017a; 1934. However, A. handidi from Upadhyay, 2017b; Upadhyay, 2018a; Ophiocephalus punctatus and A. nicolli Upadhyay, 2019). Parasites also interfere from Gobius giuris were identified by to physiological function of hosts Pande (1934, 1937, 1938). Dollfus (1949) including digestions and nutrition of described an ophthalmoxiphidiocercaria hosts, metabolism, lesions of the developing from rediae in sphaeriid alimentary canal, damage reproductive bivalves as the cercarial stage of the type and nervous system (Upadhyay, 2017c; species A. isoporum (Looss, 1894; 1902). Upadhyay, 2018b; Upadhyay et al., Further Kaw (1950) reported A. 2019a; Duan et al., 2021). Parasitic nemachilus from Nemachilus kashmirensis diseases, either alone or in conjunction after decade of consecutive investigation. with other environmental stresses, may During 1950s to 1960s Gupta had influence weight or reproduction of the explored the genus Allocreadium and host, alter population characteristics published A. thapari from Rita rita and A. and/or affect economic importance and mehri from Rhychobdella aculeate (Gupta,

Bulletin of Pure and Applied Sciences / Vol.40A (Zoology), No.1 /January-June 2021 177 Sushil Kumar Upadhyay and Babita

1950, 1951, 1953, 1956, 1961, 1962). rohita, however Gupta and Puri (1980) The trematodes A. raipurensis from recorded A. calbasii from L. calbasu and Clarias batrachus and A. spindale from A. manteri from Anabas testudineus. Mastacembelus armatus were extracted Meanwhile Khan (1981) reported A. jainin and reported by Saxena (1958). from fish Wallago attu, and A. mrigalai Meanwhile during working with O. from Cirrhinus mrigala in 1981 from punctatus, Srivastava reported A. Lucknow, Uttar Pradesh. A. tigarai was ophiocephali (1960). At the same duration reported by Bhadauria and Dandotia various scientist across the country (1986). In early 21st century, A. tonsi from contributed a lot to the taxonomic Clupisoma garua and A. bimaculatusi from diversity of Allocreadiun trematodes and Ompok bimaculatum was reported (Singh, recovered A. dollfusi, A. singhi and A. 2009). In the same year A. hirani from fish Barbus tor (Rai, 1962), A. bundelkhandensis and A. punctatai hetropneustusius from fish Hetropneustes recovered from Channa sp. of Jhansi, fossilis (Agarwal, 1963, 1964, 1966) and Uttar Pradesh (Sen and Siddiqui, 2010). Kakaji (1968, 1969a, 1969b) explored and A new species of trematode A. tori from published A. catlai from Catla catla, A. freshwater fish Tor putitora was reported fasciatusi from Trichogaster fasiatus and by Anjum et al. (2014). The redescription A. gupti from R. rita. On the other hand A. of parasite A. handiai was published on kasmirensis from Schizothorax niger was the basis of molecular analysis of the investigated by Fotedar and Dhar (1974) conserved gene and in silico approaches from Kashmir. Further, A. fotedari from S. (Chaudhary et al., 2016). Very recently A. niger was reported by Dhar and Kharoo gomtioensis was recovered Chandra et al. (1984). Later on from South India, the (2019) from Mystus tengara. All the parasitic trematodes A. fascitusi from Allocreadium species, extracted, Aplocheilus melastigma and A. hamdai recovered, described and published by from Channa punctatus were described by various scientists and scholars from (1978, 1980). Kalyankar and Deshmukh various hosts inhabiting in India were (1980) extracted A. indicum from Labeo summarized in Table. 1.

Table 1: Biodiversity checklist of Allocreadium species Looss, 1894 from various hosts in India

S.No. Hosts Parasites Authors 1. Cyprinus carpio Allocreadium sp. Looss, 1894, 1900 2. Rhynchobatus Allocreadium annandelei Southwell and Prasad, 1913 djiddensis 3. Leuciscus indicus Allocreadium sp. Thaper and Dayal, 1934 4. Ophiocephalus Allocreadium handidi Pande, 1934 punctatus 5. Channa punctatus, Allocreadium handiai Pande, 1937; Madhavi, 1980 Mystus tengara 6. Gobius giuris Allocreadium nicolli Pande, 1938 7. Schizothorax niger Allocreadium Kaw, 1944 crepidostomum 8. Nemachilus Allocreadium nemachilus Kaw, 1950 kashmirensis 9. Rita rita Allocreadium thapari Gupta, 1950,1951; Chandra, 2015 10. Rhynchobdella Allocreadium mehri Gupta, 1953, 1956, 1961 aculeate 11. Mastacembelus Allocreadium spindale Saxena, 1958 armatus 12. Clarias batrachus Allocreadium raipurensis Saxena, 1960 13. Ophiocephalus Allocreadium ophiocephali Srivastava, 1960 punctatus 14. Ophiocephalus Allocreadium makundi Gupta, 1961, 1962 punctatus

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15. Barbus tor Allocreadium dollfusi Rai, 1962 17. Barbus tor Allocreadium singhi Rai, 1962 18. Barbus tor Allocreadium hirani Rai, 1962 19. Hetropneustes fossilis Allocreadium Agarwal, 1963, 1964, 1966 hetropneustusius 20. Catla catla Allocreadium catlai Kakaji, 1968 21. Trichogaster fasciatus Allocreadium fasciatusi Kakaji, 1969a 22. Rita rita Allocreadium guptai Kakaji, 1969b 23. Schizothorax niger Allocreadium kashmirensis Fotedar and Dhar, 1974 24. Schizothorax niger Allocreadium fotedari Dhar and Kharoo, 1984 25. Puntius sarana Allocreadium saranai Gupta and Verma, 1976 26. Aplocheilus Allocreadium fascitusi Madhavi , 1978, 1979 melastigma 27. Labeo calbasu Allocreadium calbasii Gupta and Puri, 1980 28. Anabas testudineus Allocreadium manteri Gupta and Puri, 1980 29. Wallago attu Allocreadium jainin Khan, 1981 30. Labeo rohita Allocreadium indicum Kalyankar and Deshmukh, 1980 31. Cirrhinus mirigala Allocreadium mrigalai Khan, 1981 32. Puntius sophore Allocreadium tigarai Bhadauria and Dandotia, 1986 33. Mastacembalus Allocreadium dogri Agarwal and Sharma, 1989 armatus 34. Mastacembelus Allocreadium bengalensis Banerjee and Chandra, 1992 armatus 35. Clupisoma garua Allocreadium tonsi Singh, 2009, Singh et al., 2010 36. Ompok bimaculatum Allocreadium bimaculatusi Singh, 2009 37. Channa marulius Allocreadium Sen and Siddiqui, 2010 bundelkhandensis 38. Channa punctatus Allocreadium punctatai Sen and Siddiqui, 2010 39. Brachirus orientalis Allocreadium brachirusi Baghepour et al., 2011 40. Tor putitora Allocreadium tori Anjum et al., 2014 41. Mystus tengara Allocreadium handiai Chaudhary et al., 2016 42. Wallago attu Allocreadium wallagoensis Deolalikar, 2017 43. Channa punctatus Allocreadium gomtioensis Chandra et al., 2019 44. Mystus tengara Allocreadium ramai Chandra et al., 2019

GLOBAL SCENARIO OF ALLOCREADIUM markewitschi (Koval, 1949); A. dogieli LOOSS (Koval, 1950), A. carparum (Odening, 1959), A. papiligerum (Rees, 1968) were As Allocreadioides (Yamaguti, 1971), studied and reported by Moravec 1984 Creadium (Looss, 1900), Macrolecithus (2001). Meanwhile A. lobatum (Wallin, (Hasegawa and Ozaki, 1926) and 1909), A. ictaluri (Pearse, 1924), A. Neollocreadium (Akhmerov, 1962) were pseudotritoni (Rankin, 1937) and A. some synonymies of Allocreadium (Looss, alloneotenicum (Wootton, 1957) were 1894). It is the most common parasitic extracted and documented from Northern trematode species found in the gut of American hosts. It was reported that freshwater fishes inhabiting Asia, Europe, sphaeriid clams were the first and Africa, North America, Japan china, etc. arthropods found to be second (Shimazu, 1992; Shimazu and intermediate hosts for all these four North Hashimoto, 1999; Caira and Bogea, 2005; American Allocreadium sp. (Schell, 1985). Shimazu, 2008; Shimazu et al., 2011; About more than 20 species of Shimazu et al., 2016). The six species of Allocreadium was reported in China from Allocreadium from Czechoslovakia the southern drainage basin, mainly including A. isoporum (Looss, 1902); A. Yangtze and Minjiang rivers by different transversale (Szidat, 1938), A. parasitologists during past years

Bulletin of Pure and Applied Sciences / Vol.40A (Zoology), No.1 /January-June 2021 179 Sushil Kumar Upadhyay and Babita investigation (Wang, 1983; Wang, 1984; Gao et al., 2008). The Allocreadium Zhang and Yang, 1994; Lu and Wu, 1996; species documented worldwide (excluding Feng and Wang, 1997; Wu et al., 2006; India) so far summarized in Table 2.

Table 2: Global biodiversity checklist of Allocreadium species Looss, 1894 from various hosts

S.No. Hosts Parasites Authors Locality 1. Cyprinid fish, Looss, 1894, 1902; United States Barbatula barbatula Moravec, 1992; of Russia Petkeviciute et al., (USSR) 2018 2. Marine Fishes Allocreadium atomon Odhner, 1901 United Kingdom (UK) 3. Marine host Allocreadium Stossich, 1901 Lebanon pegorchis 4. Vertebrates hosts Allocreadium alacre Stossich, 1905a USSR and UK 5. Vertebrates hosts Allocreadium mormyri Stossich, 1905b USSR and UK 6. Vertebrates hosts Allocreadium Stossich, 1905c USSR and UK umbrinae 7. Semotilus Allocreadium wallini Wallin, 1909 Canada, atromaculates United States (US) 8. Aquatic vertebrates Allocreadium pallens Wallin, 1909 Canada, US 9. Semotilus Allocreadium lobatum Wallin, 1909; Canada, North atromaculates, S. Willis, 2001, 2002; America, US corporalis Curran et al., 2006 10. Vertebrate host Allocreadium fowleri Leiper and UK Atkinson, 1914 11. Fish hosts Allocreadium chuscoi Pearse, 1920 Venezuela 12. Vertebrate host Allocreadium MacCallum, 1921 USSR priacanthi 13. Aquatic hosts Allocreadium ictaluri Pearse, 1924 North America 14. Opsariichthys Allocreadium hasu Ozaki, 1926; Central Japan uncirostris Yamaguti, 1954 uncirostris 15. Zacco platypus, Allocreadium Ozaki, 1926, Central Japan Gasterosteus japonicum Yamaguti, 1971 aculeatus leiurus 17. Misgurnus Allocreadium gotoi Hasegawa and Central Japan anguillicaudatus Ozaki, 1926; Shimazu, 1988, 2017 18. Plecoglossus Allocreadium Kataoka and Central Japan altivelis altivelis incertaesedis Momma, 1934 19. Carassius arassius, Allocreadium Rankin, 1937 North America Leuciscus cephalus pseudotritoni 20. Cyprinus carpio, Allocreadium Szidat, 1938; Poland, Misgurnus fossilis transversale Popiolek et al., Czechoslovakia 2003 21. Ompok bimaculatus Allocreadium Pande, 1939 Bangladesh mahaseri 22. Cyprinus carpio Allocreadium Koval, 1949; 1966, Ukraine, USSR markewitschi Grabda, 1971 23. Alburnus alburnus Allocreadium album Koval, 1950 Ukraine 24. Alburnus alburnus Allocreadium dogieli Koval, 1950; Ukraine, USSR Wierzbicka, 1977

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25. Macrognathus Allocreadium mehrai Gupta, 1953 Bangladesh aculeatus 26. Carassius carassius Allocreadium dubium Koval, 1957; 1966 Ukraine, USSR 27. Leuciscus cephalus Allocreadium Bykhovskaya, USSR macrochis 1987 28. Alestes Allocreadium sp. Thomas, 1957; West Africa, macrolepidotus, Shimazu et al., Japan Fresh water fish 2016 29. Aquatic hosts Allocreadium Wootton, 1957 North America alloneotenicum 30. Hydroporus Allocreadium Peters, 1957; Bray Great Britain, rufifrons neotenicum et al., 2012; Camp, Bangladesh, Pisidium sp., 1992; Petkeviciute Norway Aquatic hosts et al., 2018 31. Cyprinus carpio Allocreadium Odening, 1959; Czechoslovakia carparum Moravec, 1984, 2001 32. Cyprinid fish Allocreadium Akhmerov, 1960a USSR elongatum 33. Cyprinid fish Allocreadium Akhmerov, 1960a USSR erythroculteris 34. Marine fish Allocreadium maculate Akhmerov, 1960a USSR 35. Marine fish Allocreadium Akhmerov, 1960a USSR pseudaspii 36. Hypophthalmichthys Allocreadium Akhmerov, 1960b USSR molitrix hypophthalmichthydis 37. Clarias spp. Allocreadium Beverley-Burton, Rhodesia mazoensis 1962 38. Vertebrate hosts Allocreadium Roytman, 1963; USSR hemibarbi Vainutis, 2020 39. Cyprinus carpio Allocreadium Rees, 1968; Czechoslovakia papiligerum Moravec, 1984, 2001 40. Barbus bynni Allocreadium Saoud et al., 1974 Sudan sudanensis 41. Tribolodon Allocreadium tosai Shimazu, 1988 Central Japan hakonensis; Salvelinus leucomaenis leucomaenis 42. Freshwater fish Allocreadium species Junyi, 1991 China 43. Rhynchocypris Allocreadium Shimazu, 1992 Central Japan percnurus, brevivitellatum Gasterosteus aculeatus leiurus 44. Percichthys Allocreadium Shimazu et al., Argentina colhuapiensis patagonicum 2000 45. Oncorhynchus Allocreadium lucyae Williams et al., Alahama, mykiss, Clinostomus 1992; Ernest et al., Florida funduloides 1993 46. Glossogobius giuris Allocreadium Banerjee and Bangladesh glossogobium Chandra, 1992 47. Anabas testudineus Allocreadium minutum Banerjee and Bangladesh Chandra, 1992 48. Heteropneustes Allocreadium Banerjee and Bangladesh fossilis mymensinghi Chandra, 1992 49. Glossogobius giuris Allocreadium ovatum Banerjee and Bangladesh Chandra, 1992

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50. Molluscs Allocreadium species Zhkhov, 1996 USSR 51. Gnathopogon Allocreadium Shimazu and Central Japan elongatus elongatus tribolodontis Hashimoto, 1999, 52. Phoxinus Allocreadium Shimazu, 2003 Central Japan steindachneri, G. shinanoense elongatus elongatus 53. Phoxinus Allocreadium Shimazu, 2003 Central Japan steindachneri, G. aburahaya elongatus elongates 54. Galaxias maculatus Allocreadium pichi Flores et al., 2004 Argentina 55. Nipponocypris Allocreadium sp. Shimazu, 2005, Central Japan temminckii, 2008 Tribolodon hakonensis 56. Abbottina rivularis Allocreadium Gao et al., 2008 China danjiangensis 57. Brachirus orientalis Allocreadium Bagherpour et al., Persian Gulf brachirusii 2011 58. Tanakia lanceolata Allocreadium Shimazu et al., Central Japan lanceolatum 2011 59. G. elongatus Allocreadium tamoroko Shimazu and Central Japan elongatus Urabe, 2013 60. Vertebrate host Allocreadium Vainutis, 2020 USSR khankaiensis

CONCLUSIONS fishes. Therefore, elementary knowledge of these parasites in the society could help Allocreadium Looss is the parasitic in the healthy and disease free trematodes and most commonly found in aquaculture system. The authors wish to aquatic vertebrates of India and all over suppose that current review might be the world. It is a digenean trematode helpful in the strategic management of which causes deterioration in the food aquaculture for sustainable development. value of fish, transmitted to human Further research work should be beings and affect the general public continued to clarify the biodiversity of fish health. These parasites use the fish for parasites. the purpose of shelter, food and destruct more or less each and every organ Funding Support resulting deformities in development, This research received no external growth, metabolism, digestive, funding. reproductive, nervous system and ultimately result in their mortality. Thus Conflicts of Interest the parasitic helminthes are deteriorating The authors declare no conflict of interest. the aquaculture industry in terms production, food security and economy. Acknowledgements Although there are many heartening Authors are thankful to Head Department studies have been done on the parasitic of Biotechnology, Maharishi helminthes but there are serious Markandeshwar (Deemed to be deficiencies in checklist to work out the University), Mullana-Ambala (HR), India biodiversity Allocreadium Looss (Digenea: for his kind acquiescence and Allocreadiidae). The present study based encouragement to carry out research on the literature survey and tabulated 44 work. species of Allocreadium from India and 60 species from outside India. The findings REFERENCES showed that these trematodes have immense adaptability hence occupying 1. Agarwal, S.C. and Sharma, S.K. very wide range of hosts from (1989). On a new digenetic invertebrates to vertebrates. In India trematode, Allocreadium dogri n. sp. these are most commonly reported from from the intestine of fresh water fish

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