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

Lernanthropids (Copepoda: Siphonostomatoida), 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: bavmaran@gmail.com; bavmaran@ums.edu.my]

Received 30 May 2016 ; revised 21 July 2016

Sixteen species of parasitic copepods (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, Taxonomy, Lernanthropidae, Ecology, Prevalence, First record, India.]

Introduction Parasitic copepods are common on cultured and

wild marine fin fishes and there is a vast literature describing their taxonomy and host ranges1,2. The family Lernanthropidae is one of the dominant families of the order Siphonostomatoida comprising more than 150 species and they are infested mostly on gill filaments of the host fishes1,3,4. Lernanthropus is one of the dominant genera of the family Lernanthropidae infecting marine fishes in India, consists of 44 species and most of the species are host-specific1,3,5. Lernanthropids can cause pathological effects on fishes and can directly feed on gills and blood of the host fish, in particular Lernanthropus krøyeri caused high mortalities in European seabass6. It caused respiratory failure and severe stress in cultured fishes7.

In our recent study on parasitic copepods of southeast coast of India, number of copepods was collected from marine fishes. The family Lernanthropidae, here we report has been found with six genera out of total eight genera of this family. The objectives of the present study was to reveal the infestation, prevalence and mean intensity of

lernanthropids collected from southeast coast of India. In addition, season wise ecological study was carried out for limited number of species, since many fish hosts were not available throughout the seasons. New host records have also been discussed. Materials and Methods

The present study was carried out for three years from January 2011 to December 2013 in Tamil Nadu along the southeast coast of India. Marine fishes were collected from two landing centers. Nagapattinum (Station 1: 10o 45’ N; 79o 46’ E) and Parangipettai (Station 2: 11o 30’ N; 79o 46’ E). Fishes were caught through gill net and long line fishery. They were brought to laboratory to investigate the parasitic copepod infestation. Parasites were removed from the host using fine forceps and preserved in 70 % ethanol. Further the samples were studied using a microscope (Olympus). The prevalence and mean intensity of the parasite infestation were calculated. Parasites were identified according to its morphological features1,5,8. Photographs were taken using a digital camera (Nikon-D-40). All host fishes were identified using Fish Base9. Prevalence and mean intensity were

RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA)

911

calculated10,11. Two-way ANOVA statistical analysis was performed in the ecological aspects of parasitic copepods. Voucher specimens are deposited at the museum of Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai, India. Results

Sixteen species of lernanthropids (Copepoda: Siphonostomatoida) including six different genera

(Lernanthropinus Do, Lernanthropsis Do, Lernanthropus de Balinville, Mitrapus Song & Chen, Norion von Nordmann, Sagum Wilson) (Table 1), of the family Lernanthropidae were collected from the gill filaments of marine fishes of southeast coast of India. The six genera are: Lernanthropinus (2), Lernanthropsis (1), Lernanthropus (9), Mitrapus (1), 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 intensity

Maximum intensity

Voucher specimens

Lernanthropinus Do (in Ho & Do, 1985)

Lernanthropinus forficatus (Redkar, Rangnekar et Murti, 1949)

Trichiurus savala (Cuvier, 1829)

Gills 3-4.5 (3.8 ± 0.5) 17.3 3.2 7 CASMB-35

Lernanthropinus sphyraenae (Yamaguti & Yamasu, 1959)

Mene maculata (Bloch and Schneider, 1801)

Gills 3.6-4.3 (3.9 ± 0.4) 67.4 4.8 11 CASMB-36

Lernanthropsis Do (in Ho & Do, 1985)

Lernanthropsis mugilii (Shishido, 1898)

Mugil cephalus Linnaeus, 1758

Gills 7.6-9.2 (8.6 ± 0.6) 98 15.8 36 CASMB-37

Lernanthropus (de Blainville, 1822)

Lernanthropus corniger (Yamaguti, 1954)

Megalaspis cordyla (Linnaeus, 1758)

Gills 2.6-3.1 (2.8 ± 0.2) 28 3.1 12 CASMB-38

Lernanthropus dussumieria Gnanamuthu, 1949

Stolephorus indicus (van Hasselt, 1823) and Dussumieria acuta Valenciennes, 1847

Gills 2.6-3.1 (2.8 ± 0.2) 37.3 2.7 16 CASMB-39

Lernanthropus latis Yamaguti, 1954

Lates calcarifer (Bloch, 1790)

Gills 6-8.3 (7.2 ± 0.9) 76.5 8.5 29 CASMB-40

Lernanthropus lativentris Heller, 1865

Lethrinus harak (Forsskål, 1775)

Gills 2.3-4.5 (3.6 ± 0.8) 34.6 4.1 8 CASMB-41

Lernanthropus leiognathi Tripathi, 1962

Leiognathus lineolatus (Valenciennes, 1835)

Gills 2.5-4.7 (3.6 ± 0.9) 35.5 2.7 9 CASMB-42

Lernanthropus otolithi Pillai, 1963

Daysciaena albida (Cuvier, 1830)

Gills 2.4-4.3 (3.3 ± 0.8) 15.2 2.7 10 CASMB-43

Lernanthropus polynemi Richiardi, 1881

Eleutheronema tetradactylum (Shaw, 1804)

Gills 6.2-8.6 (7.5 ± 1.1) 31.2 2.4 13 CASMB-44

Lernanthropus sillaginis Pillai, 1963

Sillago sihama (Forsskål, 1775)

Gills 2.1-3.5 (2.7 ± 0.6) 22 3.7 11 CASMB-45

Lernanthropus tylosuri Richiardi, 1880

Tylosurus crocodilus crocodilus (Peron and Lesueur, 1821)

Gills 5.1-7.4 (6.7 ± 0.7) 41.7 2.6 9 CASMB-46

Mitrapus Song and Chen, 1976

Mitrapus heteropodus (Yu, 1933)

Tenualosa toli (Valenciennes, 1847)

Gills 7.5-8.9 (7.9 ± 1) 48.3 4.6 12 CASMB-48

Norion von Nordmann, 1864 Norion priacanthi (Kirtisinghe, 1956)

Priacanthus hamrur (Forsskål, 1775)

Gills 3.2-4.3 (3.7 ± 0.5) 80.8 4 21 CASMB-49

Sagum (Wilson, 1913)

Sagum epinepheli (Yamaguti & Yamasu, 1960)

Epinephelus fasciatus (Forsskål, 1775)

Gills 3.2-4.5 (3.8 ± 0.6) 8.2 5.7 7 CASMB-50

Sagum folium Ho, Liu et Lin, 2011

Lutjanus russelli (Bleeker, 1849)

Gills 2.6-4.2 (3.4 ± 0.6) 16.3 3.1 9 CASMB-51

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

912

hosts are given: Lernanthropinus forficatus Redkar, Rangnekar & Murti (Host: Trichiurus savala), L. sphyraenae Yamaguti & Yamasu (Host: Mene maculata); Lernanthropsis mugilii Shishido (Host: Mugil cephalus); Lernanthropus corniger Yamaguti (Host: Megalaspis cordyla), L. dussumieria Gnanamuthu (Hosts: Dussumieria acuta and Stolephorus indicus), L. latis Yamaguti (Host: Lates calcarifer), L. lativentris Heller (Host: Lethrinus harak), L. leiognathi Tripathi (Host: Leiognathus lineolatus), L. otolithi Pillai (Host: Nibea albida), L. polynemi Richiardi (Host: Eleutheronema tetradactylum), L. sillaginis Pillai (Host: Sillago sihama), L. tylosuri Richiardi (Host: Tylosurus crocodilus crocodilus); Mitrapus heteropodus Yü (Host: Tenualosa toli); Norion priacanthi Kirtisinghe (Host: Priacanthus hamrur); Sagum epinepheli Yamugati & Yamasu (Epinephelus fasciatus) and Sagum folium Ho, Liu and Lin (Host: Lutjanus ruselli) (Figs. 1- 3 ).

Ecological notes on four lernanthropids Among sixteen species, season wise study

was carried out for four species including three species of Lernanthropus and one species of Norion (L. dussumieria, L. polynemi, L. leiognathy and N. priacanthi) for three years. Prevalence was higher in postmonsoon than premonsoon seasons. But mean intensity showed no much variation with the season (Fig. 4-7).Through 2-way ANOVA statistical analysis we found significant (P<0.001) interaction between prevalence and seasons for all four species, but it was only one species for mean intensity (Table 2).

Lernanthropus dussumieria A total of 18,202 individuals were examined out of

them 6,895 were infested. The overall prevalence and mean intensity were 37.85 % and 2.28, respectively. Season wise high prevalence of 73.4 % and mean intensity of 3 was observed in postmonsoon season of 2011.

Fig. 2—Lernanthropus lativentris, dorsal view (a) ventral view (b); Lernanthropus leiognathi, dorsal view (c) ventral view (d); Lernanthropus otolithi, dorsal view (e) ventral view (f); Lernanthropus polynemi, female dorsal view (g) ventral view (h), male dorsal view (i); Lernanthropus sillaginis, dorsal view (j) ventral view (k); Lernanthropus tylosuri, dorsal view (l), ventral view (m).

Fig. 1—Lernanthropinus forficatus, dorsal view (a), ventral view(b); Lernanthropinus sphyraenae, female dorsal view (c), ventralview (d), male dorsal view (e), ventral view (f); Lernanthropsismugilii, female dorsal view (g), ventral view (h), male dorsal view(i), ventral view (j); Lernanthropus corniger, dorsal view (k),ventral view (l); Lernanthropus dussumieria, dorsal view (m),ventral view (n); Lernanthropus latis (o).

Fig. 3—MitrapSagum epinephpriacanthi, dorview (g), ventra

R

pus heteropodusheli, dorsal vie

rsal view (e), venal view (h).

F

RAJA et al.: LER

, dorsal view (aew (c), ventral ntral view (f); Sa

Fig. 4—Prevale

Fig. 5—Mean int

RNANTHROPID

a), ventral view view (d); Nor

agum folium, do

ence of parasitic

tensity of parasit

DS (COPEPODA

(b); rion

orsal

LernaA t

them parasiwise in po(17.5 The hpost m2.2 du

LernaA t

them prevalof 2010.98 wise during(1.6) Nagap

c infestation from

tic infestation fro

A: SIPHONOST

anthropus leiototal of 17,796186 (34.8

ites were collhigher infe

stmonsoon o%) in pre-m

higher mean monsoon in uring premons

anthropus polytotal of 11,12

3,527 werlence of 62.2011 at Paran

% in monsoohigher mean

g summer inwas observ

pattinam.

m Parangipettai (

om Parangipetta

OMATOIDA)

ognathi 2 individuals%) were inflected (mean

estation (62.9of 2011 at Pamonsoon of 2

intensity 3 2011 at Nag

soon in 2013

lynemi. 3 individualsre infested. 2 % was obsngipettai andon of 2013 atn intensity

n 2011 at Paved during m

(2011-2013)

ai (2011-2013)

s were examinfested. Totally

intensity 2.89 %) was arangipettai a2013 at Parawas observe

gapattinam aat Nagapattin

s were examinSeason w

erved in posd low prevat Parangipetta(2.98) was

arangipettai amonsoon in

913

ned out of y, 17,174

8). Season observed

and lower angipettai. ed during and lower nam.

ned out of wise high

tmonsoon alence of ai. Season observed

and lower 2013 at

914

Norion priacA total of

them 15,886was 81.85 %collected frointensity wa93.1 % wasNagapattinampost-monsoo

Table 2—Stati

species

L. polynemi L. leiognathi L. dussumeiria N. priacanthi

canthi. f 19,451 indiv6 were infes% and a totaom the infestas 4. Seasons observed dum and meanon at 2011. S

Fi

stical analysis oNagap

Stati

F value

0.002 0.128 0.044 02.056

INDIA

viduals were eted. The oveal of 63,976ted fishes. Th

n wise higheruring post-mn intensity wSignificant in

Fig. 6—Prevale

ig. 7—Mean inte

f four species ofattinam and Para

Inf

ion

P value F va

0.964 30.20.725 17.60.836 21.90.171 26.4

AN J. MAR. SC

examined, outerall prevalen

6 parasites whe overall mer prevalence onsoon 2011

was 4.96 durnteractions w

ence of parasitic

ensity of parasit

f Lernanthropidaangipettai from 2

festation

Season St

alue P value F

26 <0.001 67 <0.001 98 <0.001 45 <0.001

CI., VOL. 47, NO

t of nce

were ean

of 1 at ring

were

observintens Discu

Thetwo lawere LernaDo w

infestation from

ic infestation fro

ae (prevalence an2011-2013 show

tation and season

F value P value

0.335 0.8 0.117 0.9490.159 0.9220.295 0.828

O. 04, APRIL 20

ved between sity.

ussion e genus Lernateral plates a

transferred anthropinus gwere synony

m Nagapattinam

om Nagapattinam

nd mean intensitwing p values (<0

n Station

e F value P val

1.54 0.231.76 0.200.83 0.3

0.164 0.6

018

seasons and

nanthropinus and eight spe

to Lernantgibbosus (Piymised with

(2011-2013)

m (2011-2013)

ty with stations a0.001 – significa

Mean int

Seaso

lue F value P

32 8.59 03 3.42 7 7.06

69 18.14 <

prevalence a

was formed ecies of Lernathropinus12.llai) and L.

L. temminc

and seasons) colant)

tensity

on Station

P value F value

0.001 1.320.043 0.2050.003 0.831

<0.001 2.41

and mean

based on anthropus Recently, sauridae

ckii (von

llected from

n and season

e P value

0.3 0.892 0.496

0.105

RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA)

915

Nordmann) based on its morphological features4 and two new species of Lernanthropinus were identified from Japan, which makes the total number of Lernanthropinus species to eight13, 14.

In this study, two species of Lernanthropinus have been reported. Lernanthropinus forficatus was first reported from Bombay (=Mumbai), west coast of India15 and later 5,16 from the host fish Lepturacanthus savala (Cuvier) (=Trichiurus savala Cuvier). It was also reported from Trichiurus lepturus Linnaeus off Gulf of Thailand with prevalence and mean intensity of 33.33 % and 1.5, respectively17. Lernanthropinus sphyraenae was first reported from the gill filaments of Sphyraena pinguis Günther off Japan18. It was later reported from Sri Lanka collected from S. obtusata19 and also from Mene maculata (Bloch & Schneider) off Taiwan20. It is a new record of occurrence from India and it is collected from two different families of host fishes such as Sphyraenidae and Menidae (see: Table 1).

The genus Lernanthropsis was adopted by Do in Ho & Do simultaneously with the former species based on the absence of plate-like structure on the trunk. There are two species have so far been recognized such as Lernathropsis mugilii (Shishido) from the Indo-west Pacific region12 and L. mugilis (Brian) from the Mediterranean region13. Both lernanthropids are host-specific to mullets (Mugilidae). Lernanthropsis mugilii was first reported from Taiwan21. Later, it was reported from Japan22 and west coast of India5 and hence, this is a first report from the southeast coast of India. Recently, L. mugilii collected it from the gill filaments of Mugil cephalus Linnaeus off Japan14 and Taiwan20.

The genus Lernanthropus has been found with more than 100 species and well distributed around the world13. In this study, we report nine species collected from the south east coast of India. Lernanthropus corniger was first reported from the gill filaments of Megalapis cordyla (Linnaeus) off Japan23. Tripathi24 reported from Rastrelliger kanagurta (Cuvier) and Pillai25 reported from west coast of India. Recently, Al-Niaeem et al. 26 reported this species from Carangoides malabaricus (Bloch & Schneider) and M. cordyla off Iraq, with the prevalence of 1.7 % and 1.4 %, respectively and mean intensity of 1.0 in both the hosts. In this study, this species was collected from M. cordyla. Lernanthropus dussumieria was first described from the gill filaments of Dussumieria acuta Valenciennes off Madras, east coast of India27.

Later Pillai28 reported it from Kerala coast. In the present study, Stolephorus indicus (van Hasselt) is added as a new host for this species. The overall prevalence and mean intensity were 37.85 % and 2.28, respectively. Season wise high prevalence and mean intensity was observed in postmonsoon season of 2011. There is no study on the ecology of L. dussumieria. Lernanthropus latis was first reported from the gill filaments of Lates calcarifer (Bloch)23. It was also reported from Sri Lanka18 and Thailand29. In Malaysia, 100 % prevalence with the intensity ranged between 1 and 18 was reported for L. latis infecting the cage-cultured L. calcarifer30 and from north Australia it was reported with the prevalence of 80-100 % in wild and cultured L. calcarifer with the mean intensity ranged from 3 to 631. In the present study also the prevalence and intensity were 86.7 % and 5.8, respectively. Lernanthropus lativentris was first reported from Lutjanus vitta (Quoy & Gaimard) off the Indian Ocean32. Later, it was reported from Japan15. Reimer33 reported on the gills of Thyrsitoides marlayi Fowler from Mozambique. Pillai5 found on the Lethrinus rhodopterus (Forsskål) from the west coast of India. In this study, it is a new host record of Lethrinus harak (Forsskål) from the Bay of Bengal, south east coast of India. The same species was reported from Lethrinus rhodopterus and Lutjanus vita34.

Lernanthropus leiognathi was first described from the gill filaments of Secutor ruconius (Hamilton) from India24 and later redescribed this species from the west coast of India5. In the present study, the host fish Leiognathus lineolatus (Valenciennes) is considered as a new host record. It was also reported from Taiwan3. Season wise higher infestation (62.9 %) was observed in postmonsoon of 2011 at Parangipettai and lower (17.5 %) during pre-monsoon in 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 otolithi was first described from Otolithes argenteus (Cuvier) off the west coast of India25. It was also reported from Taiwan from Pterotolithus maculatus (Cuvier) and Pennahia pawak (Linnaeus)3. In this study, Daysciaena albida is considered as a new host record. Lernanthropus polynemi was first reported from Eleutheronema tetradactylum (Shaw)35. It was described as L. lappaceus15,24,36,37. Later, it was redescribed as L. polynemi by synonymising with L. lappaceus and L. trifoliatus38. Recently this species

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

916

was reported as L. lappaceus off Taiwan3. 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. Mean intensity (2.98) was high in summer in 2011 at Parangipettai and low (1.6) in monsoon in 2013 at Nagapattinam.

Lernanthropus sillaginis was first described from Sillago sihama (Forsskål, 1775) off the west coast of India25. It was reported from Priacanthus tayenus (Richardson, 1846) off Thailand29 and Taiwan3. In this study, Sillago vincenti McKay, 1980 is considered as a new host record. Lernanthropus tylosuri was first described by Richiardi36. It was misidentified as L. cornutus from Sri Lanka39. Cressey and Collette40 reported it from several host fishes: Platybelone argalus (Lesueur), Strongylura anastomella (Valenciennes), S. exilis (Girard), S. incisa (Valenciennes), S. leiura (Bleeker), S. marina (Walbaum), S. strongylura (van Hasselt), S. timucu (Walbaum), S. urvillii (Valenciennes), Tylosurus acus (Lacepede), T. punctulatus (Günther) and T.crocodilus crocodilus (Peron & Lesueur). It was also reported from T. acus (Lacepede) and T. crocodilus crocodilus (Peron & Lesueur) from southern Africa41. Raibaut et al.42 reported from the Mediterranean in the gill filaments of T. acus imperialis (Rafinesque). Recently it was reported from S. leiura from the west coast with the prevalence 70 %43, which is almost similar to the present study from T. crocodilus. Tavares et al.44 reported this species from T. acus with the prevalence and mean intensity are 48.4 % and 2.5 respectively with the maximum intensity of 6.

Mitrapus heteropodus was first described as Lernanthropus heteropodus. Song and Chen45 redescribed it from Clupanodon punctatus (Temminck & Schlegel), C. thrissa (Linnaeus) off China and named as Mitrapus heteropodus. Ho & Do2 reported it from Japan from Konosirus punctatus (Temminck & Schlegel). Recently, Ho et al.3 reported this species from the gill filaments of Nematalosa nasus (Bloch) off Taiwan. In this study, it is a first record of occurrence from India.

Norion priacanthi was first described as Lernanthropus priacanthi and Aethon priacanthi from Sri Lanka46. Pillai47 reported it from India collected from Priacanthus hamrur (Forsskål). Ho & Kim29 reported this species from Gulf of Thailand and later from Taiwan3. Ho et al.20 revised this species as

Norion priacanthi. The overall prevalence was 81.85 % and the mean intensity was 4. Season wise high prevalence of 93.1 % and mean intensity of 4.96 was observed in postmonsoon 2011 at Nagapattinam.

Sagum epinepheli was first described as Pseudolernanthropus epinepheli collected from the grouper Epinephelus sp. off Japanese coast48. Pillai & Sebastian49 redescribed it as S. epinepheli. Later, it was reported from the groupers of Taiwan E. akaara and E. awoara3. Sagum folium was first described from Taiwan collected from the gill filaments of Paracaesio caerulea (Katayama)3. In this study Lutjanus russellii (Bleeker) is added as a new host record from India. Conclusion

Most of the lernanthropids are well distributed in both east and west coasts of India. Many reports were pertained only to west coast of India (Arabian Sea) and few from east coast (Bay of Bengal). However, in this study, we reported 16 species of lernanthropids from south east coast of India. Some species have also been reported from Sri Lanka, the Indian Ocean. Still, more detailed studies are needed on lernanthropids and other parasitic copepods as well50. Apparently more number of collections could enhance the biodiversity of parasitic copepods in Indian waters and redescriptions are desperately needed for most of these reported parasitic copepods. Acknowledgements

The author (K.R) acknowledge the SERB-DST, Government of India, for the award of National Post Doctoral Fellow (F.No. PDF/2016/000584). Our sincere thanks to The Principal, Government Arts College, Chidambaram (K.R & N.R). This work was supported by a year 2016 grants of Nakdonggang National Institute of Biological Resources, “Genetic Diversity Research of Freshwater Biological Resources” to UWH. Reference

1 Boxshall G A, & Halsey S H, An Introduction to Copepod Diversity, vol 1& 2. (The Ray Society, London) 2004, pp. 966.

2 Johnson, S.C., Treasurer, J.W., Bravo, S., Nagasawa, K. and Kabata, Z., A review of the impact of parasitic copepods on marine aquaculture. Zool. Stud., 43(2004) 229–243.

3 Ho, J-s., Liu, W.C. and Lin, C.L., Six species of the Lernanthropidae (Crustacea: Copepoda) parasitic on marine fishes of Taiwan, with a key to 18 species of the family known from Taiwan. Zool. Stud., 50(2011) 611–635.

RAJA et al.: LERNANTHROPIDS (COPEPODA: SIPHONOSTOMATOIDA)

917

4 Venmathi Maran, B.A., Moon, S.Y., Adday, T.K., Khamees, N.R. and Myoung, J.-G., Three new records of copepods (Siphonostomatoida) parasitic on marine fishes of Iraq, including the relegation of two species of Lernanthropinus to Lernanthropinus temminckii (Nordmann, 1864). Acta Parasitol., 59(2014) 139–152.

5 Pillai N K, Parasitic copepods of Marine fishes. In: The Fauna of India, (Zoological Survey of India, Calcutta) 1985, pp. 900.

6 Henry, M.A., Alexis, M.N., Fountoulaki, E., Nengas, I. and Rigos, G., Effects of a natural parasitical infection (Lernanthropus krøyeri) on the immune system of European sea bass, Dicentrarchus labrax L. Para. Immunol., 31(2009) 729-740.

7 Toksen, E., Lernanthropus krøyeri van Beneden, 1851 (Crustacea: Copepoda) infections of cultured sea bass (Dicentrarchus labrax L.). Bull. Europ. Ass. Fish Pathol., 27(2)(2007) 49.

8 Kabata Z, Parasitic Copepoda of British Fishes. (The Ray Society, London) 1979, pp. 468.

9 Froese, R. and Pauly, D., FishBase: World Wide Web electronic publication. Available from: http://. Fishbase Orginal version (2016), (accessed 5/2016)

10 Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M. and Schad, G.A., The use of ecological terms in parasitology (report of an ad hoc Committee of the American Society of Parasitologists). J. Parasitol., 68(1982) 131–133.

11 Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W., Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol., 83(1997) 575–583.

12 Ho, J-s. and Do, T. T., Copepods of the family Lernanthropidae parasitic on Japanese marine fishes, with a phylogenetic analysis of the lernanthropid genera. Rep. Sado Mar. Biol. Stat, Niigata Univ., 15 (1985) 31–76.

13 WoRMS Editorial Board. Lernanthropidae Kabata, 1979. In: Walter T C, & Boxshall G, (2014). World of Copepods database. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p= taxdetails&id=135526 (2016), on 2016-05-20.

14 Izawa, K., Some new and known species of the Lernanthropidae (Copepoda, Siphonostomatoida) parasitic on the branchial lamellae of Japanese actinopterygian fishes, with revision of two known species of the family and discussion on the insemination mode in the Siphonostomatoida. Crustaceana., 87(2014) 1521-1558.

15 Redkar, M.V., Rangnekar, P.G. and Murti, N.N., Four new species of parasitic copepods from the marine fishes of Bombay. J. Univ. Bombay., 18(1949) 36–50.

16 Yamaguti, S., Parasitic Copepoda and Branchiura of fishes. Interscience Publication, New York, London & Sydney, (1963) pp 1104.

17 Purivirojkul, W. and Areechon, N., A survey of parasitic copepods in Marine fishes from Gulf of Thailand, Chon Buri Province. J. Nat. Sci., 42(2008) 40–48.

18 Yamaguti, S. and Yamasu, T., Parasitic copepods from fishes of Japan with descriptions of 26 new species and remarks on two known species. Biol. J. Okayama Univ., 5(1959) 89–165.

19 Kirtisinghe, P., A review of the parasitic copepods of fish recovered from Ceylon with descriptions of additional forms. Bull. Fish. Res. Stat. Ceylon., 17(1964) 45–132.

20 Ho, J-s., Liu, W.C. and Lin, C.L., Six species of lernanthropid copepods (Siphonostomatoida) parasitic on marine fishes of Taiwan. J. Fish. Soc. Taiwan., 35(2008) 251–280.

21 Shishido, I., Parasitic copepod, Lernanthropus. Zool. Magaz., 10(1898) 120–126.

22 Shiino, S.M., Copepods parasitic on Japanese fishes. 8 The Anthosomidae. Rep. Fac. Fish. Pref. Univ. Mie., 2(1955) 50–69.

23 Yamaguti, S., Parasitic copepods from fishes of Celebes and Borneo. Publ. Seto Mar. Biol. Lab., 3(1954) 375–398.

24 Tripathi, Y.R., Parasitic copepods from Indian fishes III: Family Anthosomatidae and Dichelesthidae. Proc. 1st All- India Cong. Zool., 2(1962) 191–217.

25 Pillai, N.K., Copepods parasitic on south Indian fishes. Family Anthosomidae. 1. J. Bombay Nat. Hist. Soc., 60(1963) 655–670.

26 Al-Niaeem, K.S., Al-Azizz, S.A. and Al-Ataby, F.H., The first record of the copepod Lernanthropus corniger Yamaguti, 1954 parasitizing two carangid fishes in northwest of the Arab Gulf, Iraq. Ekologija., 59(2013) 95–98.

27 Gnanamuthu, C.P., Two male parasitic copepods from Madras. Ann. Mag. Nat. Hist., 2(1949) 359–367.

28 Pillai, N.K., Copepods parasitic on south Indian fishes. A review. Proc. Symp. Crustacea, 5(1967) 1556–1680.

29 Ho, J-s. and Kim, I.H., Lernanthropid copepods (Siphonostomatoida) parasitic on fishes of the Gulf of Thailand. Syst. Parasitol., 58(2004) 17–21.

30 Chu, K.B., Rashid, N.M. and Abd Rani, N.R., Infestation of gill copepod Lernanthropus latis (Copepoda: Lernanthropidae) and its effect on cage-cultured Asian sea bass Lates calcarifer. Trop. Biomed., 29(2012) 443450.

31 Brazenor, A.K. and Hutson, K.S., Effect of temperature and salinity on egg hatching and description of the life cycle of Lernanthropus latis (Copepoda: Lernanthropidae) infecting barramundi, Lates calcarifer. Parasitol. Int., 62(2013) 437–447.

32 Heller C, Reise der Osterreichischen Fregatta Novara um die Erde in den Jahren 1857, 1858, 1859. Zoologischer Theil, vol. 2, pb. 3, Crustacean., 1868, pp 280.

33 Reimer, L.W., Parasitic copepods of fishes from the coast of Mozambique. Wiad. Parazytol., 32(1986) 505–506.

34 Kabata, Z., Lernanthropus lativentris Heller, 1865 (Copepoda: Lernanthropidae) of recognised as a new species. Acta Parasitol., 50(2005) 352–354.

35 Richiardi, S., Contribuzione alla fauna d’Italia. 1. Catalogo sistematico dei crostacei che vivono sul corpo degli animali aquatici. In: Catalog degli Espozitioni e della Cosa Esposte, Espozitione internationale di Pesca in Berlino, Pisa, (1880) 147–152.

36 Wilson, C.B., Descriptions of new species of parasitic copepods in the collections of the United States National Museum. Proc. United States Nat. Mus., 42(1912) 233–243.

37 Pillai, N.K., Notes on copepods parasitic on South Indian marine fishes. J. Mar. Bio. Ass. India., 8(1966) 123–140.

38 Piasecki, W. and Hayward, C.J., Redescription of the fish parasite Lernanthropus polynemi Richiardi, 1881 (Copepoda: Siphonostomatoida) and relegation of two congeners to synonymy. Syst. Parasitol., 52(2002) 137–144.

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

918

39 Kirtisinghe, P., Parasitic copepods of fish from Ceylon. II. Parasitology., 29(1937) 435–452.

40 Cressey, R.F. and Collette, B.B., Copepods and needle fishes: a study in host-parasite relation- Ships. Fish. Bull. Fish and Wildlife Ser., 68(1970) 347–432.

41 Dippenaar, S.M., Reported siphonostomatoid copepods parasitic on marine fishes of southern Africa. Crustaceana., 77(2005) 1281–1328.

42 Raibaut, A., Combes, C. and Benoit, F., Analysis of the parasitic copepod species richness among Mediterranean fish. J. Mar. Syst., 15(1998) 185–206.

43 Aneesh, P.T., Sudha, K., Helna, A.K., Arshad, K., Anilkumar, G. and Trilles, J.P., Simultaneous multiple parasitic crustacean infestation on banded needlefish, Strongylura leiura (Belonidae) from the Malabar coast, India. Int. J. Sci. Res. Publ., 3(2013) 1–9.

44 Tavares, L.E.R., Bicudo, A.J.A. and Luque, J.L., Metazoan parasites of needlefish Tylosurus acus (Lacepede, 1803) (Osteichtyes:Belonidae) from the coastal zone of the state of Rio De Janeiro, Brazil. Rev. Brasil. Parasitol. Vet., 13(2004) 36– 40.

45 Song, D.X. and Chen, G.X., Some parasitic copepods from marine fishes of China. Acta Zool. Sini., 22(1976) 406–424.

46 Kirtisinghe, P., Parasitic copepods of fish from Ceylon. IV. Parasitology., 46(1956) 14–21.

47 Pillai, N.K., Description of a new species of Norion (Copepoda, Anthosomatidae) and a redescription of the type species, N. expansus von Nordmann. Crustaceana., 15(1968) 1–14.

48 Yamaguti, S. and Yamasu, T., New parasitic copepods from Japanese fishes. Publ. Seto Mar. Biol. Lab., 8(1960) 141–152.

49 Pillai, N.K. and Sebastian, M.J., Redescription of Sagum epinepheli (Yamaguti & Yamasu) with comments on the validity of Pseudolernanthropus (Copepoda, Anthosomatidae). Crustaceana., 13(1967) 73–80.

50 Raja, K. Saravanakumar, S., Gopalakrishan, A., Vijayakumar A., Hwang, U.W. and Venmathi Maran, B.A., Taxonomy and ecology of pennellids of the genus Lernaeenicus Le Sueur (Copepoda, Siphonostomatoida) and its checklist from India. Zootaxa. 4174(2016) 192–211.