Indian Journal of Geo Marine Sciences Vol. 47 (04), April 2018, pp. 910-918

Lernanthropids (Copepoda: ), Parasitic on Fishes from Southeast Coast of India

Raja, K.1,2, Rajendran, N1, Saravanakumar, A.2, Gopalakrishnan, A.2, Vijayakumar, R.2, & Venmathi Maran, B.A.3* 1PG & Research Department of Zoology, Government Arts College, Chidambaram, Tamil Nadu, India 2Center of Advanced Study in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai 608 502, Tamilnadu, India 3Endangered Marine Species Research Unit (UEMS), Borneo Marine Research Institute, Universiti Malaysia Sabah, Kota Kinabalu, Jalan UMS 88400, Sabah, Malaysia *[E-mail: [email protected]; [email protected]]

Received 30 May 2016 ; revised 21 July 2016

Sixteen species of parasitic (Siphonostomatoida) including six different genera of the family Lernanthropidae Kabata were collected from marine fishes of southeast coast of India. All fishes were collected from the fishing ports of Nagapattinam and Parangipettai, Tamil Nadu, southeast coast of India for three years from January 2011 to December 2013. Off 16 identified species, two species of Lernanthropinus, one Lernanthropsis, nine Lernanthropus, one Mitrapus, one Norion and two Sagum were recorded. All these ectoparasitic copepods were recovered from the gill filaments of the host. Ecological study (season wise) was carried out for four species of lernanthropids for three years. Prevalence was higher in postmonsoon than premonsoon seasons. However, the mean intensity was not observed with much variation between seasons. Through statistical analysis we found significant interaction between prevalence and seasons for four species (P<0.001). It is a first record of the occurrence for Mitrapus heteropodus.

[Keywords: Marine fish, Parasitic copepods, , Lernanthropidae, Ecology, Prevalence, First record, India.]

Introduction lernanthropids collected from southeast coast of India. Parasitic copepods are common on cultured and In addition, season wise ecological study was carried wild marine fin fishes and there is a vast literature out for limited number of species, since many fish describing their taxonomy and host ranges1,2. The hosts were not available throughout the seasons. family Lernanthropidae is one of the dominant New host records have also been discussed. families of the order Siphonostomatoida comprising more than 150 species and they are infested mostly on Materials and Methods gill filaments of the host fishes1,3,4. Lernanthropus is The present study was carried out for three years one of the dominant genera of the family from January 2011 to December 2013 in Tamil Nadu Lernanthropidae infecting marine fishes in India, along the southeast coast of India. Marine fishes were consists of 44 species and most of the species are collected from two landing centers. Nagapattinum host-specific1,3,5. Lernanthropids can cause (Station 1: 10o 45’ N; 79o 46’ E) and Parangipettai pathological effects on fishes and can directly feed on (Station 2: 11o 30’ N; 79o 46’ E). Fishes were caught gills and blood of the host fish, in particular through gill net and long line fishery. They were Lernanthropus krøyeri caused high mortalities in brought to laboratory to investigate the parasitic European seabass6. It caused respiratory failure and infestation. Parasites were removed from the severe stress in cultured fishes7. host using fine forceps and preserved in 70 % ethanol. In our recent study on parasitic copepods of Further the samples were studied using a microscope southeast coast of India, number of copepods was (Olympus). The prevalence and mean intensity of the collected from marine fishes. The family parasite infestation were calculated. Parasites were Lernanthropidae, here we report has been found with identified according to its morphological features1,5,8. six genera out of total eight genera of this family. The Photographs were taken using a digital camera objectives of the present study was to reveal the (Nikon-D-40). All host fishes were identified using infestation, prevalence and mean intensity of Fish Base9. Prevalence and mean intensity were RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA) 911

calculated10,11. Two-way ANOVA statistical analysis (Lernanthropinus Do, Lernanthropsis Do, was performed in the ecological aspects of parasitic Lernanthropus de Balinville, Mitrapus Song & Chen, copepods. Voucher specimens are deposited at the Norion von Nordmann, Sagum Wilson) (Table 1), of museum of Centre of Advanced Study in Marine the family Lernanthropidae were collected from Biology, Annamalai University, Parangipettai, India. the gill filaments of marine fishes of southeast coast

Results of India. The six genera are: Lernanthropinus (2), Sixteen species of lernanthropids (Copepoda: Lernanthropsis (1), Lernanthropus (9), Mitrapus (1), Siphonostomatoida) including six different genera Norion (1) and Sagum (2). There are 16 species and its

Table 1—Sixteen species of Lernanthropids (Copepoda, Siphonostomatoida, Lernanthropidae) and its ecological information from south east coast of India. Copepods Host Site Size (mm) Prevalence Mean Maximum Voucher (%) intensity intensity specimens Lernanthropinus Do (in Ho & Do, 1985) Lernanthropinus forficatus (Redkar, Trichiurus savala Gills 3-4.5 (3.8 ± 0.5) 17.3 3.2 7 CASMB-35 Rangnekar et Murti, 1949) (Cuvier, 1829) Lernanthropinus sphyraenae Mene maculata Gills 3.6-4.3 (3.9 ± 0.4) 67.4 4.8 11 CASMB-36 (Yamaguti & Yamasu, 1959) (Bloch and Schneider, 1801) Lernanthropsis Do (in Ho & Do, 1985) Lernanthropsis mugilii Mugil cephalus Linnaeus, Gills 7.6-9.2 (8.6 ± 0.6) 98 15.8 36 CASMB-37 (Shishido, 1898) 1758 Lernanthropus (de Blainville, 1822) Lernanthropus corniger (Yamaguti, Megalaspis cordyla Gills 2.6-3.1 (2.8 ± 0.2) 28 3.1 12 CASMB-38 1954) (Linnaeus, 1758) Lernanthropus Stolephorus indicus (van Gills 2.6-3.1 (2.8 ± 0.2) 37.3 2.7 16 CASMB-39 dussumieria Gnanamuthu, 1949 Hasselt, 1823) and Dussumieria acuta Valenciennes, 1847 Lernanthropus latis Lates calcarifer Gills 6-8.3 (7.2 ± 0.9) 76.5 8.5 29 CASMB-40 Yamaguti, 1954 (Bloch, 1790) Lernanthropus lativentris Lethrinus harak Gills 2.3-4.5 (3.6 ± 0.8) 34.6 4.1 8 CASMB-41 Heller, 1865 (Forsskål, 1775) Lernanthropus leiognathi Leiognathus lineolatus Gills 2.5-4.7 (3.6 ± 0.9) 35.5 2.7 9 CASMB-42 Tripathi, 1962 (Valenciennes, 1835) Lernanthropus otolithi Pillai, Daysciaena albida Gills 2.4-4.3 (3.3 ± 0.8) 15.2 2.7 10 CASMB-43 1963 (Cuvier, 1830) Lernanthropus polynemi Richiardi, Eleutheronema Gills 6.2-8.6 (7.5 ± 1.1) 31.2 2.4 13 CASMB-44 1881 tetradactylum (Shaw, 1804) Lernanthropus sillaginis Sillago sihama Gills 2.1-3.5 (2.7 ± 0.6) 22 3.7 11 CASMB-45 Pillai, 1963 (Forsskål, 1775) Lernanthropus tylosuri Tylosurus crocodilus Gills 5.1-7.4 (6.7 ± 0.7) 41.7 2.6 9 CASMB-46 Richiardi, 1880 crocodilus (Peron and Lesueur, 1821) Mitrapus Song and Chen, 1976 Mitrapus heteropodus Tenualosa toli Gills 7.5-8.9 (7.9 ± 1) 48.3 4.6 12 CASMB-48 (Yu, 1933) (Valenciennes, 1847) Norion von Nordmann, 1864 Norion priacanthi Priacanthus hamrur Gills 3.2-4.3 (3.7 ± 0.5) 80.8 4 21 CASMB-49 (Kirtisinghe, 1956) (Forsskål, 1775) Sagum (Wilson, 1913) Sagum epinepheli Epinephelus fasciatus Gills 3.2-4.5 (3.8 ± 0.6) 8.2 5.7 7 CASMB-50 (Yamaguti & Yamasu, 1960) (Forsskål, 1775) Sagum folium Ho, Liu et Lin, Lutjanus russelli Gills 2.6-4.2 (3.4 ± 0.6) 16.3 3.1 9 CASMB-51 2011 (Bleeker, 1849)

912 INDIAN J. MAR. SCI., VOL. 47, NO. 04, APRIL 2018

hosts are given: Lernanthropinus forficatus Redkar, Ecological notes on four lernanthropids Rangnekar & Murti (Host: Trichiurus savala), L. Among sixteen species, season wise study sphyraenae Yamaguti & Yamasu (Host: Mene was carried out for four species including three maculata); Lernanthropsis mugilii Shishido (Host: species of Lernanthropus and one species of Norion Mugil cephalus); Lernanthropus corniger Yamaguti (L. dussumieria, L. polynemi, L. leiognathy and (Host: Megalaspis cordyla), L. dussumieria N. priacanthi) for three years. Prevalence was higher Gnanamuthu (Hosts: Dussumieria acuta and in postmonsoon than premonsoon seasons. But mean Stolephorus indicus), L. latis Yamaguti (Host: Lates intensity showed no much variation with the season calcarifer), L. lativentris Heller (Host: Lethrinus harak), (Fig. 4-7).Through 2-way ANOVA statistical analysis L. leiognathi Tripathi (Host: Leiognathus lineolatus), L. we found significant (P<0.001) interaction between otolithi Pillai (Host: Nibea albida), L. polynemi prevalence and seasons for all four species, but it was Richiardi (Host: Eleutheronema tetradactylum), L. only one species for mean intensity (Table 2). sillaginis Pillai (Host: Sillago sihama), L. tylosuri Richiardi (Host: Tylosurus crocodilus crocodilus); Lernanthropus dussumieria Mitrapus heteropodus Yü (Host: Tenualosa toli); Norion A total of 18,202 individuals were examined out of priacanthi Kirtisinghe (Host: Priacanthus hamrur); them 6,895 were infested. The overall prevalence and Sagum epinepheli Yamugati & Yamasu (Epinephelus mean intensity were 37.85 % and 2.28, respectively. fasciatus) and Sagum folium Ho, Liu and Lin (Host: Season wise high prevalence of 73.4 % and mean Lutjanus ruselli) (Figs. 1- 3 ). intensity of 3 was observed in postmonsoon season of 2011.

Fig. 1—Lernanthropinus forficatus, dorsal view (a), ventral view (b); Lernanthropinus sphyraenae, female dorsal view (c), ventral Fig. 2—Lernanthropus lativentris, dorsal view (a) ventral view (b); view (d), male dorsal view (e), ventral view (f); Lernanthropsis Lernanthropus leiognathi, dorsal view (c) ventral view (d); mugilii, female dorsal view (g), ventral view (h), male dorsal view Lernanthropus otolithi, dorsal view (e) ventral view (f); (i), ventral view (j); Lernanthropus corniger, dorsal view (k), Lernanthropus polynemi, female dorsal view (g) ventral view (h), ventral view (l); Lernanthropus dussumieria, dorsal view (m), male dorsal view (i); Lernanthropus sillaginis, dorsal view (j) ventral ventral view (n); Lernanthropus latis (o). view (k); Lernanthropus tylosuri, dorsal view (l), ventral view (m). RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA) 913

Lernanthropus leiognathi A total of 17,792 individuals were examined out of them 6186 (34.8 %) were infested. Totally, 17,174 parasites were collected (mean intensity 2.8). Season wise higher infestation (62.9 %) was observed in postmonsoon of 2011 at Parangipettai and lower (17.5 %) in pre-monsoon of 2013 at Parangipettai. The higher mean intensity 3 was observed during post monsoon in 2011 at Nagapattinam and lower 2.2 during premonsoon in 2013 at Nagapattinam.

Lernanthropus polynemi. A total of 11,123 individuals were examined out of them 3,527 were infested. Season wise high prevalence of 62.2 % was observed in postmonsoon of 2011 at Parangipettai and low prevalence of 10.98 % in monsoon of 2013 at Parangipettai. Season wise higher mean intensity (2.98) was observed Fig. 3—Mitrapus heteropodus, dorsal view (a), ventral view (b); Sagum epinepheli, dorsal view (c), ventral view (d); Norion during summer in 2011 at Parangipettai and lower priacanthi, dorsal view (e), ventral view (f); Sagum folium, dorsal (1.6) was observed during monsoon in 2013 at view (g), ventral view (h). Nagapattinam.

Fig. 4—Prevalence of parasitic infestation from Parangipettai (2011-2013)

Fig. 5—Mean intensity of parasitic infestation from Parangipettai (2011-2013) 914 INDIAN J. MAR. SCI., VOL. 47, NO. 04, APRIL 2018

Fig. 6—Prevalence of parasitic infestation from Nagapattinam (2011-2013)

Fig. 7—Mean intensity of parasitic infestation from Nagapattinam (2011-2013)

Table 2—Statistical analysis of four species of Lernanthropidae (prevalence and mean intensity with stations and seasons) collected from Nagapattinam and Parangipettai from 2011-2013 showing p values (<0.001 – significant) species Infestation Mean intensity Station Season Station and season Station Season Station and season F value P value F value P value F value P value F value P value F value P value F value P value L. polynemi 0.002 0.964 30.26 <0.001 0.335 0.8 1.54 0.232 8.59 0.001 1.32 0.3 L. leiognathi 0.128 0.725 17.67 <0.001 0.117 0.949 1.76 0.203 3.42 0.043 0.205 0.892 L. dussumeiria 0.044 0.836 21.98 <0.001 0.159 0.922 0.83 0.37 7.06 0.003 0.831 0.496 N. priacanthi 02.056 0.171 26.45 <0.001 0.295 0.828 0.164 0.69 18.14 <0.001 2.41 0.105

Norion priacanthi. observed between seasons and prevalence and mean A total of 19,451 individuals were examined, out of intensity. them 15,886 were infested. The overall prevalence was 81.85 % and a total of 63,976 parasites were Discussion collected from the infested fishes. The overall mean The genus Lernanthropinus was formed based on intensity was 4. Season wise higher prevalence of two lateral plates and eight species of Lernanthropus 93.1 % was observed during post-monsoon 2011 at were transferred to Lernanthropinus12. Recently, Nagapattinam and mean intensity was 4.96 during Lernanthropinus gibbosus (Pillai) and L. sauridae post-monsoon at 2011. Significant interactions were Do were synonymised with L. temminckii (von RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA) 915

Nordmann) based on its morphological features4 and Later Pillai28 reported it from Kerala coast. In the two new species of Lernanthropinus were identified present study, Stolephorus indicus (van Hasselt) is from Japan, which makes the total number of added as a new host for this species. The overall Lernanthropinus species to eight13, 14. prevalence and mean intensity were 37.85 % and In this study, two species of Lernanthropinus have 2.28, respectively. Season wise high prevalence and been reported. Lernanthropinus forficatus was first mean intensity was observed in postmonsoon season reported from Bombay (=Mumbai), west coast of of 2011. There is no study on the ecology of India15 and later 5,16 from the host fish Lepturacanthus L. dussumieria. Lernanthropus latis was first reported savala (Cuvier) (=Trichiurus savala Cuvier). It was from the gill filaments of Lates calcarifer (Bloch)23. It also reported from Trichiurus lepturus Linnaeus off was also reported from Sri Lanka18 and Thailand29. In Gulf of Thailand with prevalence and mean intensity Malaysia, 100 % prevalence with the intensity ranged of 33.33 % and 1.5, respectively17. Lernanthropinus between 1 and 18 was reported for L. latis infecting sphyraenae was first reported from the gill filaments the cage-cultured L. calcarifer30 and from north Australia of Sphyraena pinguis Günther off Japan18. It was later it was reported with the prevalence of 80-100 % in wild reported from Sri Lanka collected from S. obtusata19 and cultured L. calcarifer with the mean intensity ranged and also from Mene maculata (Bloch & Schneider) from 3 to 631. In the present study also the prevalence off Taiwan20. It is a new record of occurrence from and intensity were 86.7 % and 5.8, respectively. India and it is collected from two different families of Lernanthropus lativentris was first reported from host fishes such as Sphyraenidae and Menidae (see: Lutjanus vitta (Quoy & Gaimard) off the Indian Table 1). Ocean32. Later, it was reported from Japan15. Reimer33 The genus Lernanthropsis was adopted by Do in reported on the gills of Thyrsitoides marlayi Fowler Ho & Do simultaneously with the former species from Mozambique. Pillai5 found on the Lethrinus based on the absence of plate-like structure on the rhodopterus (Forsskål) from the west coast of India. In trunk. There are two species have so far been this study, it is a new host record of Lethrinus harak recognized such as Lernathropsis mugilii (Shishido) (Forsskål) from the Bay of Bengal, south east coast of from the Indo-west Pacific region12 and L. mugilis India. The same species was reported from Lethrinus (Brian) from the Mediterranean region13. Both rhodopterus and Lutjanus vita34. lernanthropids are host-specific to mullets (Mugilidae). Lernanthropus leiognathi was first described from Lernanthropsis mugilii was first reported from the gill filaments of Secutor ruconius (Hamilton) from Taiwan21. Later, it was reported from Japan22 and India24 and later redescribed this species from the west west coast of India5 and hence, this is a first report coast of India5. In the present study, the host fish from the southeast coast of India. Recently, L. mugilii Leiognathus lineolatus (Valenciennes) is considered collected it from the gill filaments of Mugil cephalus as a new host record. It was also reported from Linnaeus off Japan14 and Taiwan20. Taiwan3. Season wise higher infestation (62.9 %) was The genus Lernanthropus has been found with observed in postmonsoon of 2011 at Parangipettai and more than 100 species and well distributed around the lower (17.5 %) during pre-monsoon in 2013 at world13. In this study, we report nine species collected Parangipettai. The higher mean intensity 3 was from the south east coast of India. Lernanthropus observed during post monsoon in 2011 at corniger was first reported from the gill filaments of Nagapattinam and lower 2.2 during premonsoon in Megalapis cordyla (Linnaeus) off Japan23. Tripathi24 2013 at Nagapattinam. Lernanthropus otolithi was reported from Rastrelliger kanagurta (Cuvier) and first described from Otolithes argenteus (Cuvier) off Pillai25 reported from west coast of India. Recently, the west coast of India25. It was also reported from Al-Niaeem et al. 26 reported this species from Taiwan from Pterotolithus maculatus (Cuvier) and Carangoides malabaricus (Bloch & Schneider) and Pennahia pawak (Linnaeus)3. In this study, M. cordyla off Iraq, with the prevalence of 1.7 % and Daysciaena albida is considered as a new host record. 1.4 %, respectively and mean intensity of 1.0 in both Lernanthropus polynemi was first reported from the hosts. In this study, this species was collected Eleutheronema tetradactylum (Shaw)35. It was from M. cordyla. Lernanthropus dussumieria was described as L. lappaceus15,24,36,37. Later, it was first described from the gill filaments of Dussumieria redescribed as L. polynemi by synonymising with acuta Valenciennes off Madras, east coast of India27. L. lappaceus and L. trifoliatus38. Recently this species 916 INDIAN J. MAR. SCI., VOL. 47, NO. 04, APRIL 2018

was reported as L. lappaceus off Taiwan3. Season Norion priacanthi. The overall prevalence was 81.85 % wise high prevalence of 62.2 % was observed in and the mean intensity was 4. Season wise high postmonsoon of 2011 at Parangipettai and low prevalence of 93.1 % and mean intensity of 4.96 was prevalence of 10.98 % in monsoon of 2013 at observed in postmonsoon 2011 at Nagapattinam. Parangipettai. Mean intensity (2.98) was high in Sagum epinepheli was first described as summer in 2011 at Parangipettai and low (1.6) in Pseudolernanthropus epinepheli collected from the monsoon in 2013 at Nagapattinam. grouper Epinephelus sp. off Japanese coast48. Pillai & 49 Lernanthropus sillaginis was first described from Sebastian redescribed it as S. epinepheli. Later, it Sillago sihama (Forsskål, 1775) off the west coast of was reported from the groupers of Taiwan E. akaara 3 India25. It was reported from Priacanthus tayenus and E. awoara . Sagum folium was first described (Richardson, 1846) off Thailand29 and Taiwan3. In from Taiwan collected from the gill filaments of 3 this study, Sillago vincenti McKay, 1980 is Paracaesio caerulea (Katayama) . In this study considered as a new host record. Lernanthropus Lutjanus russellii (Bleeker) is added as a new host tylosuri was first described by Richiardi36. It was record from India. misidentified as L. cornutus from Sri Lanka39. Cressey and Collette40 reported it from several host Conclusion fishes: Platybelone argalus (Lesueur), Strongylura Most of the lernanthropids are well distributed in anastomella (Valenciennes), S. exilis (Girard), both east and west coasts of India. Many reports were S. incisa (Valenciennes), S. leiura (Bleeker), pertained only to west coast of India (Arabian Sea) S. marina (Walbaum), S. strongylura (van Hasselt), and few from east coast (Bay of Bengal). However, in S. timucu (Walbaum), S. urvillii (Valenciennes), this study, we reported 16 species of lernanthropids Tylosurus acus (Lacepede), T. punctulatus (Günther) from south east coast of India. Some species have also and T.crocodilus crocodilus (Peron & Lesueur). It been reported from Sri Lanka, the Indian Ocean. Still, was also reported from T. acus (Lacepede) and more detailed studies are needed on lernanthropids 50 T. crocodilus crocodilus (Peron & Lesueur) from and other parasitic copepods as well . Apparently southern Africa41. Raibaut et al.42 reported from the more number of collections could enhance the Mediterranean in the gill filaments of T. acus biodiversity of parasitic copepods in Indian waters imperialis (Rafinesque). Recently it was reported and redescriptions are desperately needed for most of from S. leiura from the west coast with the prevalence these reported parasitic copepods. 70 %43, which is almost similar to the present study from T. crocodilus. Tavares et al.44 reported this Acknowledgements species from T. acus with the prevalence and mean The author (K.R) acknowledge the SERB-DST, intensity are 48.4 % and 2.5 respectively with the Government of India, for the award of National Post maximum intensity of 6. Doctoral Fellow (F.No. PDF/2016/000584). Our Mitrapus heteropodus was first described as sincere thanks to The Principal, Government Arts Lernanthropus heteropodus. Song and Chen45 College, Chidambaram (K.R & N.R). This work was redescribed it from Clupanodon punctatus supported by a year 2016 grants of Nakdonggang (Temminck & Schlegel), C. thrissa (Linnaeus) off National Institute of Biological Resources, “Genetic China and named as Mitrapus heteropodus. Ho & Do2 Diversity Research of Freshwater Biological reported it from Japan from Konosirus punctatus Resources” to UWH. (Temminck & Schlegel). Recently, Ho et al.3 reported this species from the gill filaments of Nematalosa Reference nasus (Bloch) off Taiwan. In this study, it is a first 1 Boxshall G A, & Halsey S H, An Introduction to Copepod Diversity, vol 1& 2. (The Ray Society, London) record of occurrence from India. 2004, pp. 966. Norion priacanthi was first described as 2 Johnson, S.C., Treasurer, J.W., Bravo, S., Nagasawa, K. Lernanthropus priacanthi and Aethon priacanthi from and Kabata, Z., A review of the impact of parasitic copepods Sri Lanka46. Pillai47 reported it from India collected on marine aquaculture. Zool. Stud., 43(2004) 229–243. from Priacanthus hamrur (Forsskål). Ho & Kim29 3 Ho, J-s., Liu, W.C. and Lin, C.L., Six species of the Lernanthropidae (Crustacea: Copepoda) parasitic on marine reported this species from Gulf of Thailand and later fishes of Taiwan, with a key to 18 species of the family 3 20 from Taiwan . Ho et al. revised this species as known from Taiwan. Zool. Stud., 50(2011) 611–635. RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA) 917

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