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Crustacea: Isopoda: Cymothoidae Zoological Studies 57: 25 (2018) doi:10.6620/ZS.2018.57-25 Open Access Agarna malayi Tiwari 1952 (Crustacea: Isopoda: Cymothoidae) Parasitising the Marine Fish, Tenualosa toli (Clupeidae) from India: Re-description/description of Parasite Life Cycle and Patterns of Occurrence Panakkool Thamban Aneesh1,2, Kappalli Sudha4,*, Ameri Kottarathil Helna3, and Gopinathan Anilkumar5 1Zoological Survey of India (ZSI), Ministry of Environment Forest & Climate Change, Govt. of India, Kolkata-700 053, West Bengal, India. E-mail: [email protected] 2Department of Aquatic Biology & Fisheries, University of Kerala, Kariavattam, Kerala, India 3Post Graduate Department of Zoology and Research Centre, Sree Narayana College, Kannur-670 007, India. E-mail: [email protected] 4Department of Animal Science, School of Biological Sciences, Central University of Kerala, Kasaragod-671316, India 5School of Biosciences and Technology, VIT University, Vellore 632014, India. E-mail: [email protected] (Received 7 December 2017; Accepted 19 April 2018; Published 7 June 2018; Communicated by Benny K.K. Chan) Citation: Aneesh PT, Sudha K, Helna AK, Anilkumar G. 2018. Agarna malayi Tiwari 1952 (Crustacea: Isopoda: Cymothoidae) parasitising the marine fish, Tenualosa toli (Clupeidae) from India: re-description/description of parasite life cycle and patterns of occurrence. Zool Stud 57:25. doi:10.6620/ZS.2018.57-25. Panakkool Thamban Aneesh, Kappalli Sudha, Ameri Kottarathil Helna, and Gopinathan Anilkumar (2018) This paper re-describes the female stage of Agarna malayi Tiwari 1952, a protandrically hermaphroditic parasitic cymothoid, and describes the remaining life cycle stages for the first time. The re-description (female phase) of A. malayi was made based on the type specimens deposited by Tiwari (1952) in the National Zoological Collections of the Zoological Survey of India (NZC-ZSI) and data obtained from several live specimens collected from Ayyikkara Fish Landing Centre (11°51'N, 75°22'E, of Malabar Coast, India) and Marina Beach (13.0500°N, 80.2824°E, Bay of Bengal, India). General morphology, mouthparts and appendages of the species’ life cycle stages such as larvae, juveniles, male and transitional stages are also reported for the first time. We closely observed 80 marine fish species belonging to 35 different families to identify the potential host of A. malayi, and only recovered the parasite from one fish, Tenualosa toli, signifying A. malayi’s oligoxenous host specificity; the prevalence and intensity of parasitisation is 17.3 and 1.86%, respectively. The present paper also discusses sequential life cycle stages of the species. Key words: Parasitic cymothoid, Lifecycle, Clupeid fish, Host-parasite interaction, India. BACKGROUND considerable interest among parasitologists and fish pathologists (Brusca 1981; Aneesh et al. Members of the family Cymothoidae Leach 2016a b). Cymothoids usually prefer specific parts 1814 are known to be obligatory parasites of of the host fish; for instance, the Nerocila Leach teleost fishes from diverse ecosystems. The 1818 and Anilocra Leach 1818 are usually found adverse effect of its parasitism has generated attached to the general body surface, species of *Correspondence: E-mail: [email protected]; [email protected] © 2018 Academia Sinica, Taiwan 1 Zoological Studies 57: 25 (2018) page 2 of 22 Cymothoa Fabricius 1793, Ceratothoa Dana 1852 juvenile and larvae (manca I and manca II). and Glossobius Schiödte and Meinert 1883 are Though the occurrence of A. malayi has found in the buccal cavity, while species of Agarna recently been reported from the Malabar Coast, Schiödte and Meinert 1884, Joryma Bowman and India (Aneesh et al. 2015), the precise information Tareen 1983, Ryukyua Williams and Bunkley- regarding their distribution and pattern of host- Williams 1994 and Mothocya Costa and Hope parasite interaction are still lacking. At this 1851 prefer the branchial cavities (Aneesh et al. juncture, this paper addresses the questions of the 2013 2015; Bruce et al. 2016). distribution, prevalence, intensity, host specific and In the literature, Cymothoid-infecting fish site specific nature of A. malayi parasitisation. An have been reported all over the world, particularly attempt was also made to discuss the sequential in South Africa (Hadfield et al. 2013 2014), South life cycle stages of A. malayi. America (Thatcher et al. 2003 2007), Europe (Trilles 1994; Horton and Okamura 2001); America (Brusca 1981; Wiliams and Bunkley-Williams MATERIALS AND METHODS 1994), Australia (Bruce 1987; Martin et al. 2015; Bruce et al. 2016), Philippines (Yamauchi et al. Live and fresh fishes were obtained from the 2005), Kuwait (Bowman and Tareen 1983), China Ayyikkara Fish Landing Centre (11°51'N, 75°22'E, (Yu and Li 2003), Malaysia (Seng and Seng 1990) Malabar Coast, India) to check for parasitisation and India (Tiwari 1952; Pillai 1964; Trilles et al. by Agarna malayi. Much care was taken to 2011; Aneesh et al. 2015). Our knowledge on collect the fishes directly from local fishermen cymothoid parasitisation of marine fishes in India and/ or fishing boats, which were just harbored still needs to be updated. to the landing centres and thereby ensured the Agarna Schioedte & Meinert, 1884, a genus reproducibility of sampling of parasites. During in the family Cymothoidae, currently include the study period of November 2009 to November four valid species: A. bengalensis Kumari, 2013, we have observed over 80 species of marine Hanumantha, Rao and Shaymasundari 1990, A. fishes belonging to 35 families for the presence cumulus (Haller 1880), A. malayi Tiwari 1952 and A. of Cymothoids. Additional collections were made pustulosa Pillai 1954. Three additional species of from Fish Landing Centre at Marina Beach, Agarna (A. brachysoma Pillai 1964, A. engraulidis Chennai (13.0500°N, 80.2824°E, Bay of Bengal, Barnard 1936 and A. tartoor Pillai 1954) were India) from March to June, 2016. Collections synonymized with Joryma Bowman and Tareen were made twice a week. Immediately after each 1983 by Bowman and Tareen (1983). collection, body parts of the fish were closely Agarna malayi Tiwari, 1952, a very poorly examined for the presence of cymothoids using known cymothoid, was described 65 years ago a hand lens. The recovered parasites and their by Tiwari (1952) based on ovigerous female hosts were brought to the laboratory and subjected specimens collected from its clupeid host fish, to detailed examination with the aid of a stereo Nematalosa nasus (Bloch, 1795), from Kolkata, microscope (Leica-S6D). The live cymothoids India. The author illustrated the dorsal and lateral were fixed in 5% formaldehyde and preserved view of the specimen and provided a description in 75% ethanol (Ramakrishna 1980; Aneesh et of mouth parts and few pereopods. Later, Pillai al. 2016a b) and subjected to detailed taxonomic (1964) transferred this species to the genus Indusa identification (Tiwari 1952) according to appropriate Schiödte and Meinert 1884 with a brief description; taxonomical keys. Total lengths of both host fish but Bowman and Tareen (1983) retained the and the parasite (A. malayi) were measured. The species under Agarna. identification of life cycle stages and classification Cymothoids exhibit protandric hermaph- of female stages were done according to roditism, so a description of their life cycle stages Bakenhaster et al. (2006) and Aneesh et al. (e.g. larvae and adults) would facilitate precise (2016b). Larval stage nomenclature followed the species identification, irrespective of the infective Atlas of Crustacean Larvae by Martin et al (2014). stages. We therefore 1) re-described females The description and the type series of A. malayi, of Agarna malayi based on the type specimens comprising the holotype and paratype, were also identified by Tiwari (1952) extant in the NZC- thoroughly examined and kept in good condition, ZSI and on the data obtained from several live extant in the NZC-ZSI. Dissection and mounting specimens collected recently; 2) describe all other of appendages were done according to Aneesh life cycle stages including male, transitionals, et al. (2016b). Mouthparts and appendages of the © 2018 Academia Sinica, Taiwan Zoological Studies 57: 25 (2018) page 3 of 22 recovered live and fresh parasite (A. malayi) were 1795) (Clupeidae) (Tiwari 1952) and Mugil carefully dissected out using a dissecting needle ophueseni (Bleeker) (= Valamugil cunnesius and a pair of fine forceps, and observed under (Valenciennes)) (Mugilidae) (Pillai 1954, 1964). microscopes (Leica DM-750 and Leica M-205A). Distribution: Kolkata (Tiwari, 1952), The specimens were microphotographed using a Travancore (Pillai 1954), Kayamkulam Lake, multi focusing stereo microscope (Leica-M205A) Kerala, southwestern coast of India (Pillai 1964), and image capturing software (Leica Application Bay of Bengal and Malabar Coast of Kerala, India Suit). The drawings of the observed mouthparts (present study). and appendages were performed using a camera Material examined: 55 ♀♀, 5 transitionals, lucida attached the microscope (Leica M-205A). 50 ♂♂, 4 juveniles, 28 manca I and 36 manca II. Fish taxonomy and host nomenclature were Type material: Holotype: 1♀ , from performed according to FishBase (Froese and Nematalosa nasus, purchased from Bow Bazar, Pauly 2017) and Catalogue of Fishes (Eschmeyer Kolkata, India; Coll. Shri Malay Kumar Datta, Reg. 2017). The prevalence (P) and intensity (I) of No. C3121/2 ZSI. recovered A. malayi were calculated by the Paratype:
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