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. 2021 Apr 8;45(4):944–951. doi: 10.1007/s12639-021-01382-1

Confirmation on the occurrence of Cymothoa indica, and first record of Norileca indica, with a note on new host records of Nerocila arres, and Nerocila depressa (Isopoda: Cymothoidae) from Odisha coast, India

Jaya Kishor Seth 1,✉, Sandeep Kumar Mohapatra 1, Swarup Ranjan Mohanty 2, Rajesh Kumar Behera 3, Anil Mohapatra 2
PMCID: PMC8556475  PMID: 34789976

Abstract

The parasitic isopod Cymothoa indica Schiöedte and Meinert, 1884 was recorded from the buccal cavity of the host Glossogobius giuris (Hamilton, 1822) collected from Chilka Lake, Odisha in 1924, but its identification was doubtful as mentioned by the author in his book on “Fauna of Chilika Lake: Tanaidacea and Isopoda”. The present report of parasitic isopod C. indica from the buccal cavity of the host Sphyraena obtusata Cuvier, 1833 collected from the water of Bay of Bengal, Gopalpur-on-Sea confirms its occurrence along the Odisha coast. The record of the isopod parasite Norileca indica (H. Milne Edwards, 1840) from the branchial cavity of the host Atule mate (Cuvier, 1833) collected from the water of Bay of Bengal, Gopalpur-on-Sea is the first record of this parasite from the coastal water of Odisha, India. The record of Nerocila arres Bowman and Tareen, 1983 from the caudal peduncle of the host fish species Terapon puta Cuvier, 1829, and the isopod N. depressa Milne Edwards, 1840 from the host fish species Megalaspis cordyla (Linnaeus, 1758) are the new host records for these respective parasites.

Keywords: Gopalpur-on-Sea, New host, New records, Parasitic Isopods

Introduction

The parasitic isopods of the family cymothoidae are recorded from different body parts of host fishes viz., buccal cavity, branchial region, body surface, and caudal peduncle. These parasitic isopods cause a range of infections to the host fishes; thereby inhibiting the growth of the host fishes and sometimes cause death of the host fishes, which is a concerned for the aquaculture productivity (Rameshkumar et al. 2013; Seth et al. 2020a, b; Seth et al. 2014; Trilles et al. 2011, 2013).

The genus Cymothoa Fabricius, 1793 includes 49 valid species across the globe and it is equal largest with the genus Anilocra Leach, 1818 under the family cymothoidae (Martin et al. 2016). Only 5 species of the genus Cymothoa are known from Indian water viz., Cymothoa bychowskyi Avdeev, 1979, C. eremita (Brünnich, 1783), C. frontalis Milne Edwards, 1840, C. indica Schiöedte & Meinert 1884, and C. parupenei Avdeev, 1979. The species C. indica is known to infect a wide range of host fishes. In India, it was documented from the Southeast coast of India (Ravichandran et al. 2019), and from West Bengal (Mishra and Nandi 1986). It was earlier recorded from the host Glossogobius giuris (Hamilton 1822) collected from Chilka Lake, Odisha in 1924. However, its identification was doubtful as mentioned by the author in his book “Fauna of Chilika Lake: Tanaidacea and Isopoda” (Chilton 1924). Therefore, the present record of the species C. indica from the host fish species S. obtusata collected from the water of Bay of Bengal, Gopalpur-on-Sea confirms the occurrence of this parasite from the costal water of Odisha. The list of hosts reported for the parsite C. indica from different localities of India is provided in Table 1.

Table 1.

Host-parasites list, host family and sampling localities of India

Isopod species Host species Host Family Locality References
Cymothoa indica Mystus gulio (Hamilton, 1822) Bagridae Parangipettai, Southeast Coast of India Rajkumar et al. (2005a)
Strongylura strongylura (van Hasselt, 1823) Belonidae Hoogly estuary, Bakkali and Sagar island, Sunderbans, West Bengal Mishra and Nandi (1986)
Parangipettai, Southeast Coast of India Rajkumar et al. (2004)
Eetroplus maculates (Bloch, 1795) Cichlidae Chennai Coast Panikkar and Aiyar (1937)
E. suratensis (Bloch, 1790) Chennai Coast Panikkar and Aiyar (1937)
Nematolosa nasus (Bloch, 1795) Clupeidae Personal observation of M. Rajkumar Rajkumar et al. (2005b)
Glossogobius giuris (Hamilton, 1822) Gobiidae Chilika Lake, Odisha Martin et al. (2016)
Oxyurichthys microlepis (Bleeker, 1849) Parangipettai, Southeast Coast of India Ravi and Rajkumar (2007)
Lates calcarifer (Bloch, 1790) Latidae Parangipettai, Southeast Coast of India Rajkumar et al. (2005b)
Siganus javus (Linnaeus, 1766) Siganidae Personal observation of M. Rajkumar Rajkumar et al. (2005b)
Sphraena obtusata Cuvier, 1829 Sphyraenidae Parangipettai, Southeast Coast of India Veerapan and Ravichandran (2000)
S. obtusata Gopalpur-on-Sea, Odisha coast Present study
Synodus myops (Forster, 1801) Synodontidae Parangipettai, Southeast Coast of India Veerapan and Ravichandran (2000)
Nerocila arres Nemipterus japonicus (Bloch, 1791) Nemipteridae Nagappatinam Trilles et al. (2013), Rameshkumar et al. (2013)
Siganus canaliculatus (Park, 1797) Siganidae Odisha coast Dev Roy et al. (2015)
Terapon puta Cuvier, 1829 Terapontidae Goapalpur-on-Sea, Odisha Coast Present study
Nerocila depressa Carangoides malabaricus (Bloch and chneider, 1801) Carangidae Parangipettai, Southeast Coast of India Rameshkumar et al. (2016)
Megalaspis cordyla (Linnaeus, 1758) Goplapur-on-Sea, Odisha Coast Present study
Selaroides leptolepis (Cuvier, 1833) Goplapur-on-Sea, Odisha Coast Seth et al. (2020a)
Parangipettai, Southeast Coast of India Rameshkumar et al. (2016)
Opisthopterus tardoore (Cuvier, 1829) Mumbai Bal and Joshi (1959)
Lagocephalus lunaris (Bloch and Schneider, 1801) Tetraodontidae Digha, West Bengal Balakrishnan and Tudu (2020)
Lepturacanthus pantului (Gupta, 1966) Trichiuridae Digha, West Bengal Balakrishnan and Tudu (2020)
Norileca indica Atula mate (Cuvier, 1833) Carangidae Goplapur-on-Sea, Odisha Coast Present Study
Selar crumenophthalmus (Bloch, 1793) Great Nicobar Island Seepana (2021)
Secutor insidiator (Bloch, 1787) Leiognathidae Visakhapatnam Behera et al. (2016)
Nemipterus randalli Russell, 1986 Nemipteridae Visakhapatnam Behera et al. (2016)
Rastrelliger kanagurta (Cuvier, 1816) Scombridae Malabar coast Aneesh et al. (2016)
Visakhapatnam Behera et al. (2016)
Shankarpur, West Bengal Ray et al. (2016)
Cochin coast Jemi et al. (2020)
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The genus Nerocila Leach 1818 of the family cymothoidae includes 43 valid species (Nagasawa and Isozaki 2019). In India, to date, only 12 species of the genus Nerocila are recorded (Ravichandran et al. 2019). The species N. arres was earlier recorded from different host fish species viz., Acanthopagrus latus (Houttuyn, 1782), Epinephelus tauvina (Forsskål, 1775), N. japonicas, N. peronii (Valenciennes, 1830), and Priacanthus hamrur (Forsskål, 1775) (Ravichandran et al. 2019) and Siganus canaliculatus (Park, 1797) (Dev Roy et al. 2015). The N. arres was recorded from the Southeast coast of India (Ravichandran et al. 2019) and from Odisha coast (Dev Roy et al. 2015). The list of hosts reported for the parasite N. arres from different localities of India is provided in Table 1. The present record of N. arres from the host fish species T. puta collected from Bay of Bengal, Gopalpur-on-Sea is the new host record for the parasite. The isopod species N. depressa was recently recorded from the coastal water of Odisha from the host Selaroides leptolepis (Cuvier, 1833) (Seth et al. 2020a). The list of hosts reported for the parasite N. depressa from different localities of India is provided in Table 1. The present record of N. depressa collected from the body of the host fish species M. cordyla is the new host record for this parasite.

The genus Norileca (Milne Edwards 1840) is represented by three species worldwide. In India, only two species viz., N. indica (H. Milne Edwards, 1840) and N. triangulata (Richardson, 1910) were reported. The species N. indica was reported from the Southeast coast, southwest coast (Ravichandran et al. 2019), West Bengal coast (Ray et al. 2016), Vishakapatnam coast (Behera et al. 2016), and from Great Nicobar Island (Seepana et al. 2021) from India. The species N. indica was reported from nine host fish species including the host A. mate (Kottarathil et al. 2019). The list of hosts for the parasite N. indica from different localities of India is provided in Table 1. The present report of the species N. indica from the host A. mate collected from the coastal water of Gopalpur-on-Sea is the first record of this parasite from the Odisha coast and confirms its occurrence along the entire east coast of  India.

Materials and methods

The host fish species along with the isopods parasites were collected through different fishing nets operation from the Bay of Bengal, Gopalpur-on-Sea, Odisha during the month of November–December, 2020 (19°14′46.37″ N and 85°53′45.25″ E). The host fish species were photographed and brought to the laboratory for future studies. The isopod parasites were gently pulled off, photographed, and kept in 70% ethanol for further studies. The hand drawing of the parasites were also carried out for better identification, and future reference. The host fish species are kept in 10% formaldehyde solution. The host fish species were identified as per standard features provided in the Fishbase (Froese and Pauly 2020). The isopods parasites were identified as per the standard taxonomic keys and features described by Ravichandran et al. (2019). All the reported isopod parasites and the host fish species are deposited and registered in the National repository of Estuarine Biology Regional Centre, Zoological Survey of India, Gopalpur-on-Sea, Odisha, India. The registration number of these isopods are prefix with “Cr” under the description section. Both male and female individuals of the isopod C. indica were collected from a single host S. obtusata. The female of the isopod N. arres was collected from a single host Nemipterus japonicus (Bloch, 1791), and the transitional stage of the same parasite was collected from a single host T. puta. The female individual of the isopod N. depressa was collected from the host M. cordyla. The female and male individuals of the isopod parasite Norileca indica were collected from the branchial cavity of the same host -08 different individual of the same host A. mate. Measurements and sex details of the hosts are provided in Table 2.

Table 2.

Measurements of hosts

Species S. obtusata T. puta M. cordyla N. japonicus A. mate (number of hosts:08)
Sex Female Female Female Male

Female: 05

Male:03
Total length (cm) 23.9 11.8 12.5 22 20.4–23.3
Standard length (cm) 20.1 9.7 10.2 18.3 16.8–18.4
Body depth (cm) 2.9 3.5 2.8 5.9 4.6–5.9
Body width (cm) 2.9 1.6 1.2 2.6 2.3–2.7
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Results

The taxonomic account and description of these parasites collected from the different host fish species during the study are provided below:

Order: Isopoda Latreille, 1817.

Family: Cymothoidae, 1818.

Genus Cymothoa Fabricius, 1793.

Cymothoa indica Schiöedte and Meinert, 1884 (Fig. 1: a1–a4).

Fig. 1.

Fig. 1

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a Cymothoa indica attached to host Sphyraena obtusata, (a1) Cymothoa indica (female) dorsal view, (a2) Cymothoa indica (female) ventral view, (a3)Cymothoa indica (male) dorsal view, (a4) Cymothoa indica (male)ventral view, b Nerocil arres attached to host Nemipterus japonicas, (b1)Nerocila arres (female) dorsal view, (b2) Nerocila arres (female) ventral view, c Nerocila arres attached to host Terapon puta, (c1) Nerocila arres (transitional stage) dorsal view, (c2) Nerocila arres (transitional stage) ventral view, d Nerocila deppresa attached to host Megalapsis cordyla, (d1) Nerocila deppresa (female) dorsal view, (d2) Nerocila deppresa (female) ventral view, e Norileca indica attached to branchial cavity of host Atule mate, (e1) Norileca indica (female) dorsal view, (e2) Norileca indica (female) ventral view, (e3) Norileca indica (male)dorsal view, (e4) Norileca indica (male)ventral view

Description of female (Fig. 1:a1–a2) (Fig. 2:a–b).

Fig. 2.

Fig. 2

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a Cymothoa indica (female) dorsal view, b Cymothoa indica (female) ventral view, c Cymothoa indica (male) dorsal view, d Cymothoa indica (male) ventral view,(e) Nerocila arres (female) dorsal view, f Nerocila arres (female) ventral view, g Nerocila arres (transitional stage) dorsal view), h Nerocila arres (transitional stage) ventral view, i Nerocila depressa (female) dorsal view, j Nerocila depressa (female) ventral view), k Norileca indica (female) dorsal view, l Norileca indica (female) ventral view, m Norileca indica (male) dorsal view, n Norileca indica (male) ventral view

Materials examined: 01(Cr-12478). The total length of the parasite is 21.5 mm and the total width is 11 mm. The length and width of cephalon are 1.5 mm, and 3 mm respectively. The numbers of perionites are 07, and numbers of pleonites are 05. The length of pleotelson is 4 mm, and its width is 7.5 mm.

Body is creamy white. Body is about 1.95 times as long as wide. Cephalon is 2 times as wider as length. Eyes visible. Antennula composed of 8 articles and the third article is longest. Antenna is having 9 articles. Pereonite 1 longest and pereonite 7 shortest in length. Pleonite 1–4 subequal in length and pleonite 5 widest. Pleonite 1 partially concealed by pereonite 7. Chromatophores present on the margin of pereonites.

Description of male (Fig. 1: a3–a4) (Fig. 2:c–d).

Materials examined: 01(Cr-12477). The total length of the parasite is 10.5 mm, and total width is 4.5 mm. The length and width of cephalon are 2 mm and 2.5 mm respectively. The numbers of pereonites are 07, and numbers of pleonites are 05. The length and width of pleotelson are 2 mm and 3 mm respectively.

Body is creamy white. Body is about 2.33 times as long as wide. Cephalon is 0.8 times as long as wide. Eyes are large, but not clearly visible. Chromatophores present on the margins of pereon and pleon. The lateral margin of pereon has chromatophores.Pleonite 1 and 2 partially concealed by perionite 7. The proximal margin of pleotelson has chromatophores.

Genus Nerocila Leach 1818

Nerocila arres Bowman and Tareen, 1983 (Fig. 1: b1–c2).

Description of female (Fig. 1: b1–b2) (Fig. 2:e–f).

Materials examined: 01 (Cr-12515). The total length of the parasite is 26 mm, and its total width is 13 mm. The length of cephalon is 3 mm and width is 4 mm. The numbers of pereonites are 07, and the numbers of pleonites are 05. The length of pleotelson is 5 mm, and its width is 5 mm.

Body is creamy whitish. Body is about 2 times as long as wide.The Cephalon is 1.33 times as wider as length. Eyes not clearly visible, and its diameter of is 1 mm. Antennula composed of 8 articles. Antenna 9 articled. perionite 2–3 smaller in length and 6–7 longest. Perionite 6–7 widest.pleonite 1 not concealed by perionite 7. Pleonite 1 longest and 2–5 subequal in length.

Description of transitional stage (Fig. 1: c1–c2) (Fig. 2:g–h).

Materials examined:01 (Cr- 12514). The total length of the parasite is 16.5 mm, and its total width is 8 mm. The length of cephalon is 2 mm, and width is 3 mm. The numbers of pereonites are 07, and the numbers of pleonites are 05. The length of pleotelson is 4 mm, and its width is 4 mm.

Body is creamy whitish. Body is about 2 times as long as wide. The cephalon is 1.5 times as wider as length. Eyes not clearly visible, diameter of eye is 0.5 mm. Other characters are similar to female.

Nerocil depressa Milne Edwards, 1840.

Description of female (Fig. 1: d1–d2) (Fig. 2:i–j).

Materials examined: 01(Cr.12479). The total length of the parasite is 15 mm, and its total width is 6 mm. The length of cephalon is 2 mm, and width is 3 mm. The numbers of pereonites are 07, and the numbers of pleonites are 05. The length of pleotelson is 2.2 mm, and its width is 3 mm.

Body is yellowish and is about 2.5 times as long as wide. Cephalon is 0.67 times as wide as long. Pleotelson is 1.36 times as long as wide. Antennula composed of 8 articles. Antenna 10 articled. Eyes not visible. Ventrolateral margins of pleonite 1 and 2 extending. None of the pleonites concealed by perionite 7. Chromatophores present on the margins of pleonites and perionites.

Norileca (Milne Edwards 1840)

Norileca indica (H. Milne Edwards, 1840) (Fig. 1: e1–e4).

Description of female (Fig. 1: e1–e2) (Fig. 2:k–l).

Materials examined: 08(Cr-12482 A-H). The total length of the parasite is 19–33 mm, and its total width is 9.5–14 mm. The length of cephalon is 2–3.5 mm and its width is 2.2–3.2 mm. The numbers of pereonites are 07, and the numbers of pleonites are 05. The length of pleotelson is 5–13 mm, and its width is 5–12 mm.

Body is brown and is about 2.0–2.36 times as elongated as width. Cephalon is 2 times as wider as length. Eyes visible, diameter of eye is 0.5–1.2 mm. Antennula composed of 8 articles. Antenna 9 articled. Lateral margin of pereonite 1 elongated and covering nearly half of the cephalon sidewise. Perenite 5 widest. Pleonites sub equal in length. Pleotelson triangualar in shape. Pleotelson width smaller than width of pleonites. Body is twisted to left or right side depending upon the site of attachment.

Description of male (Fig. 1: e3–e4) (Fig. 2:m–n).

Materials examined: 03 (Cr.12476). The total length of the parasite is 13.2–14.0 mm, and its total width is 5.0–5.5 mm. The length of cephalon is 1.0–2.0 mm and its width is 2.0 mm. The numbers of pereonites are 07, and the numbers of pleonites are 05. The length of pleotelson is 2.9–3.2 mm, and its width is 2.5–3.2 mm.

Body is brownish. Body is about 2.64–2.54 times as long as wide. Cephalon is 0.5–1 times as long as wide. Eye large and visible.diameter of eye is 1 mm. In males the diameter of eye is larger in proportion to head as compared to female. Body is not twisted. All other characters are similar to female.

Discussion and conclusion

The parasitic isopods reported so far from the coastal water of Odisha are Anilocra dimidiata Bleeker, 1857 from the host fish species Karalla

daura (Cuvier, 1829) (Seth et al. 2020a), Elthusa propinqua (Richardson, 1904) (Dev Roy and Rath 2017), Mothocya renardi (Bleeker, 1857), and M. collettei Bruce, 1986 from the host species Strongylura leiura (Bleeker, 1850) (Mohapatra et al. 2021), N. arres from the host fish species Siganus canaliculatus (Dev Roy et al. 2015), N. depressa from the host fish species Selaroides leptolepis, N. sigani Bowman and Tareen, 1983 from the fish species viz., T. theraps Cuvier, 1829, and Lutjanus lutjanus Bloch, 1790 (Seth et al. 2020a), N. phaiopleura Bleeker, 1857 from the host fish species Rastrelliger kanagurta (Seth et al. 2014), and N. sundaica (Barnard 1936), Joryma engraulidis (Barnard 1936) from the host fish species Thryssa setirostris (Broussonet, 1782) (Barnard 1936; Dev Roy and Rath 2017), J. malabaricus Aneesh, Helna and Trilles, 2018 from the host fish species Ilisha melastoma (Bloch and Schneider, 1801), J. hilsae Rameshkumar, Ravichandran and Trilles, 2011 from the host fish species I. melastoma, and J. sawayah Bowman and Tareen, 1983 from the host fish species I. melastoma (Seth et al. 2020b).

The present finding of the species C. indica confirms its occurrence in the coastal water of Odisha. The report of the isopod Norileca indica is the first record of this parasite from the coastal water of Odisha. The report of species N. arres from the host T. puta confirms a wide host range of infection of the parasite. The report of the parasite N. depressa from M. cordyla is an addition to the host list of this parasite.

Acknowledgements

Authors are thankful to authority of Berhampur University, Odisha and Director, Zoological Survey of India for providing necessary facilities to work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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