_____________________________________________________________________________________________________ *Corresponding author: Email: akv.gdcz@gmail.com; Original Research Article UTTAR PRADESH JOURNAL OF ZOOLOGY 41(10): 121-127, 2020 ISSN: 0256-971X (P) SEASONAL VARIATIONS IN PREVALENCE OF ECTOPARASITIC INFESTATION IN INDIAN MAJOR CARPS AT BALRAMPUR, U.P., INDIA SADGURU PRAKASH1 AND ASHOK KUMAR VERMA2* 1Department of Zoology, Maharani Lal Kunwari P.G. College, Balrampur, 271201, Uttar Pradesh, India. 2Department of Zoology, Goverment PG College Saidabad, Prayagraj, 221508, Uttar Pradesh, India. AUTHORS' CONTRIBUTIONS This work was carried out in collaboration between both authors. Author SP designed the study, performed the statistical analysis and wrote the protocol. Author AKV wrote the first draft of the manuscript, analyses the study and managed the literature searches. Both authors read and approved the final manuscript. Article Information Editor(s): (1) Dr. Golam Mustafa, Center for Resource Development Studies Ltd., Bangladesh. Reviewers: (1) Danilo Rodrigues Barros Brito, Instituto Federal do Maranhão – IFMA, Brazil. (2) Costache Mioara, Fish Culture Research and Development Station Nucet, Romania. (3) Jangchuk Gyeltshen, Royal Government of Bhutan, Bhutan. Received: 06 June 2020 Accepted: 12 August 2020 Published: 22 August 2020 ABSTRACT The present investigation was conducted during April 2019 to March 2020 to find out the seasonal variation in prevalence of ectoparasites of Indian major carps. Total 10 species of ectoparasites were collected from 360 fishes. Out of ten, three belong to Myxozoan (Myxobolus sp., Thelohannellus sp. and Henneguya sp.), three Ciliophporans (Trichodina sp., Tripertiella sp. and Ichthyophthirus sp.), two Monogeneans (Dactylogyrus sp. and Gyrodactylus sp.) and two Crustaceans (Ergasilus sp., and Argulus sp.). Among the different groups of ectoparasites, Myxozoan has shown highest prevalence (19.91%) throughout the year followed by Ciliophorans (17.31%), Crustaceans (9.63%) and Monogenean (1.95%). Among the ectoparasites, Myxobolus sp. is the most prevalent ectoparasites followed by Trichodina sp., Thelohannellus sp., Tripertiella sp. and Argulus sp. It was observed that the infection was the maximum during winter, moderate in summer and minimum in monsoon season. Keywords: Parasites; environmental factors; Catla catla; Labeo rohita; Cirrhinus mrigala. 1. INTRODUCTION Health of any population depends on the control of disease and maintenance of a healthy relationship between living organisms and their environment. The parasitic community of fish normally show considerable variation with the environmental conditions in which fish live [1]. Certain environmental conditions are more conducive to disease among which water temperature is one of the important criteria associated with disease outbreak. It was observed that the prevalence of the disease was Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 122 more in the winter season than the other months of the year [2]. Fishes are the aquatic vertebrates found both in marine and fresh water [3] and beneficial for human health. Fish culture is one of the most economically important applied strategies all over the world and fishes are one of the most beneficial and nutritional resources of human beings [4]. Parasitic diseases are the limiting factors in fish culture, because of increased density of fish in lentic water bodies where the fish pathogens can easily transmit from one fish to another. These pathogens may cause fish mortality in cultural fishes where the entire fish population of pond may be killed, resulting the great economic loss of fish farmers. Some parasites are serious pests in fish culture; others are probably potential threats to fish culture. On the other hand, blue revolution and success of fisheries development programme depends on the intensification of fish parasitological research, as the improvement of fish yield can mainly be achieved from healthy fish stock. Thus to prevent the economic loss and to present fish production, proper fish health management is necessary. The ectoparasites of fish constitute one of the most important problems associated with pond fish culture. Fish disasters in fish farms were caused by different ectoparasites (protozoa, monogenetic trematoda and crustacea), which have direct life cycle and facilitate translocation from host to host making huge damages to fish wealth [5]. The most important prerequisite of fish production is availability of healthy fish fingerlings of carps [6]. Because of easily availability of fish seed (fry and fingerlings) of the indigenous major carps, Catla catla, Labeo rohita and Cirrihinus mrigala have become the most common culturable freshwater fishes of eastern Uttar Pradesh. Studies on parasitic diseases of fishes particularly in this tarai region of eastern Uttar Pradesh are fragmentary [7]. Considering the above facts, the present study was aimed to find out the ectoparasitic prevalence of indigenous major carp fingerlings as well as the correlation between ectoparasitic prevalence and environmental conditions. 1.1 Study Area The study area was Balrampur town (Image 1) which is situated in North-Terai region of Uttar Pradesh adjacent to Indo-Nepal border at 27°16' N to 27°32' north latitude and 82°03'E to 82°22' east longitude and an altitude of about 113 meters above the mean sea level. The selected lentic water bodies namely Mavalal Talab, Rani Talab and Tulsidas Talab (Image 2) were small perennial fresh water ponds, situated at a distance of 596.3 m, 792.0 m and 831.6 m, to the M.L.K.P.G. College Balrampur campus. The maximum area occupied by the Mavalal Talab, Rani Talab and Tulsidas Talab was 0.8 ha, 1.38 ha and 0.9 ha, respectively. Image 1. Map of Uttar Pradesh and Balrampur District Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 123 Image 2. Satellite view of Balrampur showing study sites 2. MATERIALS AND METHODS 2.1 Fish Collection From the three fishery ponds viz, Tulsidas talab, Mavalal talab and Rani talab of Balrampur districts of eastern U.P., 120 live host or freshly dead specimen of each indigenous carp, Catla (Catla catla), Rohu (Labeo rohita) and Mrigal (Cirrhinus mrigala) were randomly sampled and collected from April 2019 to March 2020 and transported to the Ichthyology lab, Department of Zoology, M.L.K.P.G. College, Balrampur. The fishes were examined immediately after collection for detailed investigation of ectoparasites. 2.2 Examination of Host Fishes and Collection of Parasites For observation and identification of parasites, indigenous carps were collected from these three local talab (ponds). The external surface such as scales, fins, skin and fin base of host fishes were examined under a magnifying glass for ectoparasites or any kind of lesions. Then scrapping of the skin was done by a scalpel to collect the mucus in a petri dish for microscopic examination. After that gills were removed from the bronchial cavity and placed on a glass slide for microscopic examination. From this, lice, large nematodes and helminthes were collected by a hairbrush, protozoan parasites were collected from the mucus or body surface by pipette, dropper and needle in a slide. 2.3 Identification of Parasites Parasites were identified under a compound microscope and following the description and figures of Gupta [8], Yamaguti [9], Lucky [10], Kabata [11], Hafizuddin and Shahabuddin [12] and Mukherjee et al. [2]. 2.4 Prevalence Study The parasitic prevalence was estimated with the help of parasitic frequency index (PFI) which was calculated by taking the percentage of the number of hosts infected by an individual parasite species against the total number of hosts examined in a particular area under investigation. Prevalence frequency index (PFI) was estimated following the formula given by Margolis et al. [13]. Prevalence (%) = Total no. of infected  ishes Total no. of  ish host examined X 100 2.5 Study of Water Quality The water quality parameters viz, water temperature, pH, DO and hardness are directly related to fish health [2]. These were measured per month from the three local fishery ponds. The temperature and pH of water Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 124 sample were analyzed on spot by using a mercury bulb thermometer, and pH meter, respectively. Dissolved oxygen (DO) and hardness of water samples were analyzed by following standard titrimetric methods [14]. 3. RESULTS AND DISCUSSION In the present study, a total of 10 genera belong to 4 group of ectoparasites were collected from indigenous carps, Catla (Catla catlasurface feeder), Rohu (Labeo rohita -column feeder) and Mrigal (Cirrhinus mrigala bottom feeder). Among the collected parasites, three were Myxozoan parasites (Myxobolus sp., Thelohannellus sp.and Henneguya sp.), three Ciliophporans parasites (Trichodina sp., Tripertiella sp. and Ichthyophthirus sp.), two Monogeneans (Dactylogyrus sp. and Gyrodactylus sp.) and rest two were Crustaceans (Ergasilus sp., Argulus sp.). Myxozoan were found on gills and fins of host fishes except Calta where they were found only on fins. Ciliophorans were found on skin and gill but Tripertiella sp. was found only on the skin of host fishes. Monogeneans were found alive and strongly attached to gill, skin and fins base but the Dactylogyrus sp. was found gills of host fishes. Crustaceans were mostly found abundantly attached to the fin and skin and rarely on operculum (Table 1). Table 1. List of ectoparasites, host fishes and their infection sites Parasitic Group Infection sites of host fishes Catla catla Labeo rohita Cirrhinus mrigala Myxozoan Myxobolus sp. Fins Gill, Fins Gill Thelohannellus sp. Fins Gill, Fins Fins Henneguya sp. Fins Gill Ciliophorans Trichodina sp. Skin, Gill Skin, Gill Skin, Gill Tripertiella sp. Skin Skin Skin Ichthyophthirus sp. Skin, Gill Skin Monogeneans Dactylogyrus sp. Gill Gill Gill Gyrodactylus sp. Skin, Fin base Skin Crustacean Ergasilus sp. Skin, Gill Skin, Gill Skin, Gill Argulus sp. Skin, Fins, Operculum Skin, Fins base Skin, Fins, Table 2. Seasonal variation in PFI (%) of Indian major carp fingerlings Parasitic Groups PFI % of the affected Indian major carp Catla catla Labeo rohita Cirrhinus mrigala Average % PFI Monsoon season (JulyOctober) Myxozoan Myxobolus sp. 20.4 28.5 24.2 24.37 Thelohannellus sp. 11.4 15.2 13.5 13.37 Henneguya sp. 0.0 0.0 0.0 0.0 Ciliophorans Trichodina sp. 15.4 22.4 18.6 18.80 Tripertiella sp. 18.5 22.4 20.2 20.37 Ichthyophthirus sp. 0.0 0.0 0.0 0.0 Monogeneans Dactylogyrus sp. 0.0 0.0 0.0 0.0 Gyrodactylus sp. 0.0 0.0 0.0 0.0 Crustacean Ergasilus sp. 0.0 0.0 0.0 0.0 Argulus sp. 0.0 0.0 0.0 0.0 Seasonal Average % PFI 6.57 7.33 7.65 Winter season (November-February) Myxozoan Myxobolus sp. 42.8 58.6 46.4 49.27 Thelohannellus sp. 36.2 48.2 42.5 42.30 Henneguya sp. 0.0 6.2 3.4 3.20 Ciliophorans Trichodina sp. 28.3 40.2 32.5 33.67 Tripertiella sp. 25.4 32.1 28.6 28.70 Ichthyophthirus sp. 0.0 7.4 6.8 4.73 Monogeneans Dactylogyrus sp. 4.6 7.8 6.6 6.33 Gyrodactylus sp. 0.0 2.4 1.8 1.40 Crustacean Ergasilus sp. 9.4 16.4 14.8 13.53 Argulus sp. 34.2 48.8 42.6 41.87 Seasonal Average % PFI 18.09 26.81 22.60 - Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 125 Parasitic Groups PFI % of the affected Indian major carp Catla catla Labeo rohita Cirrhinus mrigala Average % PFI Summer season(March-June) Myxozoan Myxobolus sp. 25.2 33.4 27.4 28.67 Thelohannellus sp. 15.4 20.2 18.5 18.03 Henneguya sp. 0.0 0.0 0.0 0.0 Ciliophorans Trichodina sp. 20.4 30.4 24.6 25.13 Tripertiella sp. 20.5 28.4 24.2 24.37 Ichthyophthirus sp. 0.0 0.0 0.0 0.0 Monogeneans Dactylogyrus sp. 0.0 4.6 3.6 2.73 Gyrodactylus sp. 0.0 2.0 1.4 1.20 Crustacean Ergasilus sp. 0.0 0.0 0.0 0.0 Argulus sp. 0.0 4.8 2.4 2.4 Seasonal Average % PFI 8.15 12.38 10.21 Yearly Average % PFI 10.94 15.51 13.49 - Table 3. Seasonal variations in PFI % age of individual ectoparasite within the Group Parasitic Groups Seasons variations in PFI% age Monsoon Winter Summer Average % PFI Myxozoan Myxobolus sp. 24.37 49.27 28.67 34.10 Thelohannellus sp. 13.37 42.30 18.03 24.57 Henneguya sp. 0.0 3.20 0.0 1.07 Average PFI% 12.58 31.59 15.57 19.91 Ciliophorans Trichodina sp. 18.80 33.67 25.13 25.87 Tripertiella sp. 20.37 28.70 24.37 24.48 Ichthyophthirus sp. 0.0 4.73 0.0 1.58 Average PFI% 13.06 22.37 16.50 17.31 Monogeneans Dactylogyrus sp. 0.0 6.33 2.73 3.02 Gyrodactylus sp. 0.0 1.40 1.20 0.87 Average PFI% 0.0 2.58 1.31 1.95 Crustacean Ergasilus sp. 0.0 13.53 0.0 4.51 Argulus sp. 0.0 41.87 2.4 14.75 Average PFI% 0.0 55.40 0.8 9.63 Seasonal average % age PFI 6.41 27.94 8.55 - Table 4. Seasonal variations of water quality parameters of three water bodies Seasons Water Temp.(0C) Dissolved Oxygen (ppm) pH Hardness (ppm) Tulsidas Talab Monsoon 30.7 6.24 6.5 138.5 Winter 18.8 7.88 7.7 114.4 summer 27.4 7.24 8.1 125.6 Mavalal Talab Monsoon 31.0 5.81 6.4 141.5 Winter 19.1 7.15 7.4 117.4 summer 27.6 6.85 7.8 129.6 Rani Talab Monsoon 30.5 6.1 6.6 135.5 Winter 18.9 7.85 7.8 115.2 summer 27.3 7.19 8.2 123.4 Table 2 revealed that some groups and some genera of ectoparasites are totally absent in particular season, such as Crustaceans are found only in winter season and rarely in summer season. The monogeans parasites were not found during monsoon season. The Ichthyophthirus sp. of Ciliophporans and Henneguya sp. of Ciliophporans were found only during winter season. The present study also revealed that some parasites such as Henneguya sp., Ichthyophthirus sp. and Gyrodactylus sp. were host specific because Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 126 these were not infect the Catla catla (Table 2). Among the ectoparasites, Myxobolus sp. is the most prevalent ectoparasites followed by Trichodina sp., Thelohannellus sp., Tripertiella sp. and Argulus sp. These ectoparasites are the most common parasites of Indian major carps in West Bengal, India [2], which support the present findings. Sharif and Vijarungam [15] reported that Trichodina sp. is the most common ectoparasite and caused mass mortality of carp fish in nursery pond. The prevalence of ectoparasites of carp in different seasons has been presented in Tables 2 and 3. Among the different groups of ectoparasites, Myxozoan has shown highest prevalence (19.91%) throughout the year followed by Ciliophorans (17.31%), Crustaceans (9.63%) and Monogenean (1.95%). In winter season, the prevalence of ectoparasites reached at 27.94% and gradually decreased in summer (8.55%) and monsoon (6.41%). This indicates that the ectoparasitic infection changed with the change of season. All groups of ectoparasites have also been shown highest prevalence in winter followed by summer and monsoon season (Table 3). This indicates that abiotic and biotic factors of water body are responsible for infection. Mukherjee et al. [2], reported that low pH and low temperature were the major factor for spreading several parasitic diseases in fishes. The water temperature, dissolved oxygen, pH and hardness are major water quality parameters that were found related to disease infection in fishes as they fluctuate more rapidly. The seasonal variation data of these parameters have been shown in the Table 4. The ectoparasitic prevalence has shown temperature sensitivity. Ectoparasitic prevalence increases when water temperature and hardness decreases [16]. The optimum levels of dissolved oxygen and neutral pH have a positive effect on the prevalence of ectoparasites [16], which supports the present finding. During winter season, environmental conditions such as water temperature, pH, hardness and dissolved oxygen were more suitable for the growth and multiplication of parasites. Winter season had already been identified as a period of high susceptibility of fish to parasites [17,18]. According to Mukherjee et al. [2], the prevalence of the parasites was maximum during winter due to high organic load in culture ponds which induces bio-ecological stress and made fish more susceptible to the parasitic infection. The fingerlings are delicate and more susceptible to pathogenic infection because of their immature immune system [16], which corroborated with the present findings. Since the fingerlings require more O2 and due to lack of O2 they become more prone to infection. High stocking density of fingerlings is another reason for ectoparasitic diseases outbreak [1]. High stock density increases the possibility of transmission of ectoparasites from fish to fish easily. 4. CONCLUSION On the basis of present investigation, it can be concluded that the post monsoon season, i.e. winter season, along with the low water temperature, high level of dissolved oxygen, moderate pH and low hardness provides favorable environmental conditions for the ectoparasitic infections, specially Myxobolus sp. Thelohannellus sp. Trichodina sp. Tripertiella sp. and Argulus sp. Due to low water temperature, fish reduces metabolic activities, which in turn also made the fishes more susceptible during winter season towards ectoparasitic infestations. Thus, it could be concluded that the water quality has a great impact on the abundance of pathogens and their ability to survive on host. So the stocking density of fish seed and water quality parameters should be maintained properly to avoid parasitic infestation in pond fishes. ACKNOWLEDGEMENT Authors are highly grateful to the Principal and Management Committee of MLK (P.G.) College, Balrampur (U.P.) for providing necessary laboratory facilities. COMPETING INTERESTS Authors have declared that no competing interests exist. REFERENCES 1. Hossain MD, Hossain MK, Rahaman MH, Akter A and Khanom DA. Prevalence of ectoparasites of carp fingerlings at Santaher, Bogra. University Journal of Zoology, Rajshahi University. 2008;27:17-19. 2. Mukherjee D, Soni M, Sanyal KB and Dash G. Prevalence of ectoparasitic infestation in Indian major carps during winter at different blocks of South 24-Parganas District, West Bengal, India. Journal of Fisheries Science. 2019;1(1): 7-14. 3. Verma AK, Prakash S. Status of animal phyla in different kingdom systems of biological classification. International Journal of Biological Innovations. 2020;2(2):149-154. Available:https://doi.org/10.46505/IJBI.2020.2 211 4. Banerjee S, Bandyopadhyay PK. Observation on prevalence of ectoparasites in carp fingerlings in two districts of West Bengal. Journal of Parasitic Diseases. 2010;34(1):44-47. Prakash and Verma; UPJOZ, 41(10): 121-127, 2020 127 5. Al-Marjan KSN, Abdullah SMA. Some ectoparasites of the common carp (Cyprinus carpio) in Ainkawa fish hatchery, Erbil province. J. Duhok Univ. 2009;12(1):102-107. 6. Chakraborty BK, Shahroz MH, Bhuiyan AB, Bhattacharjee S, Chattoraj S. Status of Indian major carps spawns in the Halda River along with marketing and economic condition of the Fishers and related collectors. International Journal of Biological Innovations. 2019;1(2): 40-50. Available:https://doi.org/10.46505/IJBI.2019.1 202 7. Prakash S, Verma AK. Incidence of parasites in Labeo rohita (Hamilton) at Balrampur (U.P.). Life science Bulletin. 2017;14(2):181-183. 8. Gupta SP. Nematode parasites of vertebrates of East Pakistan III. Camallandidae from fishes, amphibian and reptiles. Can. J. Zool. 1959;86: 771-779. 9. Yamaguti S. Systema Helminthum-IV: Monogenea and Aspidocotylea. Interscience Publication, NewYork. 1963;699. 10. Lucky Z. Methods for the diagnosis of fish diseases. Amerind Publishing Co. Pvt. Ltd. New Delhi, New York; 1971. 11. Kabata Z. Parasites and diseases of fish cultured in the Tropics. Taylor and Francis, London and Philadelphia; 1985. 12. Hafizuddin AKM, Shahabuddin M. Parasitic monogeneans from some freshwater fishes of Comilla, Bangladesh. Chittagong Univ. Stud. Sci. 1996;20:113-126. 13. Margolis L, Esch GW, Holmer JC, Kuris AM, Schad GA. The use of ecological terms in parasitology. Journal of Parasitology. 1982;68: 131-133. 14. APHA. Standard methods for Examination of water and waste water. American Public Health Association 21st Ed. APHA, New York; 2005. 15. Sharif M, Vijiarungam AF. The occurrence of parasites at fish breeding station in peninsular Malaysia and their control. Proc. Intercont. Dev. Managem.Trop. Living Aquat. Resources. Serdang, Malaysia. 1986;68-73. 16. Mortuza M, Golam, Fahad A. Al-Misned. Prevalence of ectoparasites in crop fry and fingerlings of Rajshahi district, Bangladesh. J. Parasitic Diseases. 2015;39(2):130-133. 17. Rahman MR, Akter MA, Hossain MD. Parasitic diseases of exotic carp in Bangladesh. J. Agric. Rural Dev. 2007;5(1&2):127–134 18. Farhaduzzaman AM, Alam MM, Hossain M, Hussain MA, Rahman MH. Prevalence of parasites in the Indian major carp, Labeo rohita (Hamilton) in Rajshahi, Bangladesh. Univ. J. Zool. Rajshahi Univ. 2010;28:65–68. DOI: 10.3329/ujzru.v28i0.5290. __________________________________________________________________________________________ © Copyright MB International Media and Publishing House. All rights reserved.