Infection of the parasitic isopods on commercial fishes of the northern part of the east coast of India

The present study reports the parasitic isopod infection on commercial fishes of the northern part of the east coast of India collected during the period 2010–2015 from the marine waters of Odisha and West Bengal. During the study, 394 isopods were collected after examining 2668 fishes. These include 14 species of isopods, out of which 13 belong to 5 genera under the family Cymothoidae, and a single species Alitropus typus belongs to the family: Aegidae. Of theses, 03 species viz., Catoessa boscii, Cymothoa eremita and Nerocila loveni are first record to the northern part of east coast of India. Out of the 2668 fishes examined, 326 examples belonging to 34 species under 19 different families were infected by different isopods. Members of the host fish family Carangidae were more parasitized by isopods, followed by Clupeidae, Scoberidae, and Leiognathidae. The dominant isopods were Nerocila phaiopleura and Catoessa boschii. The total prevalence was 12.21. The prevalence was high on the host fish Alepes djedaba and lowest on Lutjanus johnii. The total infection caused by genus Alitropus was 1.52%, Anilocra was 5.07%, Catoessa was 24.87%, Cymothoa was 0.25%, Nerocila was 65.73%, and Norileca was 2.55%. The isopod prevalence was high during post-monsoon than pre-monsoon and monsoon.


Introduction
The parasitic isopods usually occur in the freshwater, estuarine and marine ecosystem, especially near the coastal environment. In these ecosystems, they play an essential role in the ecological food chain and removal of the decaying matter (Bharadhirajan et al. 2014). Besides this ecological role, the study of these isopods is also important as they cause a range of damages to the fishes, thereby threatening the fisheries sector Seth et al. 2020aSeth et al. , b, 2021. Out of the 144 known isopod families, only a few are parasitic. The family Cymothoidae is one of the most prominent families of the order Isopoda. The representative of the family is the obligate parasites, known to show a high degree of the host and site-specificity to the host fishes (Ravichandran et al. 2019). However, in some species, host specificity is weak.
The family Cymothoidae consists of more than 380 species under 43 genera worldwide (Smit et al. 2014). Of these, 48 valid species under 16 genera are reported from Indian water (Ravichandran et al. 2019). The adult forms of the family Aegidae White, 1850 of the order Isopoda, are considered temporary parasites as they often leave their host after a blood meal. Due to this nature, they have been recently classified as free-living micro-predators (Ravichandran et al. 2019). The family Aegidae includes around 152 species under 8 genera worldwide (Al-Zubaidy and Mhaisen 2014). The genus Alitropus H. Milne Edwards, 1840 is monotypic contains the only species A. typus (Yule and Sen 2004). This species primarily occurs in the coastal ecosystem's fresh water and low salinity zone (Bruce 1983).
In India, most of the reports and records on parasitic isopods are concentrated around the south-east coast of India (Ravichandran et al. 2019). There are reports on the isopods parasites from the northern part of the east coast of India (NPECI), mainly from the state of Odisha and West Bengal (Chilton 1924;Seth et al. 2014;Dev Roy et al. 2015;Behera et al. 2016;Ray et al. 2016Ray et al. , 2020Dev Roy and Rath 2017;Balakrishnan and Tudu 2020;Seth et al. 2020aSeth et al. , b, 2021Mohapatra et al. 2021), but still, a comprehensive report is lacking (Seth et al. 2020a(Seth et al. , b, 2021. Further, on the prevalence of these isopods on the host fish species, there is hardly any report from the NPECI. Therefore, this study was carried out to know the infection and prevalence of these isopods along the NPECI.

Materials and methods
During the study period (August 2010-January 2015), a routine observation (at the rate of 3-5 days per month/ seasons) of the marine fishes from different selected fish landing stations of the NPECI viz. West Bengal (Digha, Shankarpur, Junput, Hijli-Dariapur, Kakdwip-Namkhana, and Sagar Island) and Odisha (Talsari, Chandipur, Dhamra, Paradip, Puri, Chilika, and Gopalpur) were conducted. The map of the study area is provided as supplementary file. Sampling periods were divided into three seasons: premonsoon (February-May), monsoon (June-September), and post-monsoon (October-January). Fishes and isopod were collected from fish landing centers where trawl net and gill net generally operated; some samples were also collected from shore seine nets. Fishes were checked carefully for ectoparasitic infection on their body surface, fins, gill, and buccal cavity. After photography, isopods were removed from their attachment sites with the help of fine forceps and placed into 70% ethanol. The isopods were examined using Leica-EZ4 microscope. Isopods were identified according to Trilles (1975Trilles ( , 1979, Bowman and Tareen (1983), Bruce (1987), Rameshkumar et al. (2011), andTrilles et al. (2013). The prevalence was calculated according to Margolis et al. (1982). Host species identification was based on Fischer and Bianchi (1984), Talwar and Kacker (1984), Froese and Pauly (2021). Specimens were deposited and registered in the Marine Aquarium and Regional Center (MARC), Zoological Survey of India, Digha. The specimens of A. typus was deposited and registered in Estuarine Biology Regional Centre, Zoological Survey of India, Gopalpur-on-Sea, Odisha. The registered specimens along with their voucher number are presented in Table 1.The seasonal impacts of the parasites on the host were also examined.

Results
During the study, 14 species of parasitic isopods were found (Fig. 1); from those, 13 species belong to family Cymothoidae and 01 species to the family Aegidae. Out of theses 14 species, 03 species viz., Catoessa boscii, Cymothoa eremita and Nerocila loveni are first record to the NPECI. Few selected photographs of hosts and their parasites collected during the study period are presented in Fig. 2. A comprehensive list of the isopods species along with their host collected during the study period and earlier report form Indian water are presented in Table 2. During this study, it was observed that isopods parasitized 34 species of host fishes under 19 families. Number of host fish species examined and parasitized by isopods are presented in Fig. 3. Most of the isopod attached with host species mainly three regions: body surface, buccal cavity, and inside the gill membrane (Branchial parasite). Host family-wise infection by isopods is provided in Fig. 4. Member of the family Carangidae are more parasitized by the isopods followed by Clupeidae, Scomberidae, and Leiognathidae (Fig. 4). The percentage of dominating isopods genus wise and species wise are provided in Figs. 4 and 5 respectively. The dominating genus was Nerocila (Fig. 5), Nerocila phaeopleura and Catoessa boschii are the main dominant isopod in these areas (Fig. 6).The seasonal variation of isopod infection is presented in Fig. 7. The Isopod prevalence was high during October to February (post-monsoon season to early part of pre-monsoon) and very low during March to August (pre-monsoon Fig. 1 Parasitic isopods collected during the study and monsoon) (Fig. 7). The prevalence is provided in Table 3. Total prevalence was 12.21. The prevalence was highest on Alepes djedaba (34.95) and lowest on Lutjanus johnii (1.29).

Discussions and conclusion
The parasitic isopods viz., Catoessa boscii, Cymothoa eremita, and Nerocila loveni were not recorded earlier from the NPECI; therefore, this is the first materials evidence of     Barnard (1936) On several species of shoal fishes Travancore Pillai (1954) Arius maculatus Nagappatinam Trilles et al. (2013) Host ( (Table 2). As these isopods are connected with many host species during the study period (Figs. 3 and 4; Tables 2 and 3), it indicates higher diversity of fishes in the NPECI. The Nerocila is the dominating genus during the study period (Figs. 5,6), which shows the high adaptability of the species of the genus to a range of environmental conditions prevailing in these regions. The high prevalence of isopod on the host species Alepes djedaba (Table 3) may be due to the higher host-specificity of parasitic isopods for this host species in these regions.
The Isopod prevalence was high during post-monsoon than pre-monsoon and monsoon (Fig. 7). During this study, it is observed that most of the Nerocila species were ovigerous throughout the year, but the prevalence was high during post-monsoon. High prevalence during post-monsoon may be due to favourable environmental conditions in the mentioned period of the year. It is also evident from the fact that in many free-living crustaceans, post-monsoon plays a vital role in their breeding, and climatic conditions affect the reproduction of Cymothoidae (Sudha and Anilkumar 1996;Syama et al. 2010;Leonardos and Trilles 2003).
In recent times, study on the infection and prevalence of parasitic isopods on commercial fishes were reported from Paranagipettai coast, India (Bharadhirajan et al. 2014), Malabar Coast, India (Aneesh et al. 2016;Rijin et al. 2017), Mirri, East Malaysia (Anand Kumar et al. 2015Kumar et al. , 2017, Atlantic menhaden (Rose et al. 2020) and other parts of the globe as well. However, before the present report, no such comprehensive study based on the infection of parasitic isopods on the commercial fishes of NPECI was reported. Therefore, the extension of this work on the infection pattern and other aspects of the host-parasite relationship in these regions will provide more insight into the isopods biology.
Acknowledgements We would like to express our thankfulness to Director, Zoological Survey of India for providing necessary facilities to work.
Funding Not applicable.

Declarations
Conflict of interest Authors declare that they have no conflict of interest.
Research involving human participants and/or animals Since the animals are not under schedule lists/protected categories, so ethical clearance is not applicable.