Indian Journal of Geo Marine Sciences Vol. 47 (08), August 2018, pp. 1594-1600

New distributional record of Halieutaea Indica (Lophiiformes: ) from Chilika lagoon, India

Debasish Mahapatro1, R.C. Panigrahy1, Sudarsan Panda2, Subodh K. Karna3, R.K. Mishra4, S.S. Mishra5 & S.K. Mohanty6 1Department of Marine Sciences, Berhampur University, Berhampur-760007, Odisha, India 2Regional CCF, Angul-759143, Odisha, India 3CIFRI, Barrackpore, West Bengal, India 4National Centre for Antarctic and Ocean Research (NCAOR), MoES, Goa- 403804, India 5Marine Fish Section, Zoological Survey of India, Kolkata-700016, India 6Fishery Consultant, Chilika Development Authority, Bhubaneswar, India

[E. Mail: [email protected]]

Received 08 August 2016; revised 24 January 2017

The present study provides the first occurrence report of Indian hand fish, Halieutaea indica Annandale & Jenkins, 1910 from Outer Channel of the Chilika Lagoon. This bathy-demersal species is now the only member of the order Lophiiformes known to occur in this brackish water ecosystem. Its incidence for the first time in the Chilika may be attributed to change in the lagoon habitat after the opening of new lagoonal inlets, that subsequently accommodating newer species. This species is a pure marine form and might have entered the lagoon during the higher salinity phase in the lagoon. Present study further described the gut content of Halieutaea indica that comprised of benthic crab, prawn, amphipoda and free-living nematodes.

[Keywords: Indian hand fish, Ramsar site, bathydemersal, taxonomic classification, gut content, esca]

Introduction central sector with brackish water condition, southern Fishes belonging to the order Lophiiformes sector with marine to brackish water condition and outer comprised of a wide range of organisms having channel area is entirely of marine region, as it is different body morphology with an extensive connected to the sea with couple of inlets4,5. Thus, assortment of adaptation and distribution throughout fishery resource of the Chilika mostly depend up on the world, which are accommodated in 18 families1. coastal marine forms, as most of the fishes enter the The family Ogcocephalidae contains about 75 species lagoonal water from the Bay of Bengal 4,5. During the belonging to 10 genera2 of which Indian waters are last few decades, the lake has faced much pressure from known to have only 11 species in 6 genera, viz., Coelophrys (1 sp.), Dibranchus (1 sp.), Halicmetus (1 sp.), Halieutaea (5 spp.), Halieutopsis (1 sp.) and (2 spp.)3. Chilika Lagoon (19° 28’-19° 54’N and 85° 05’-85° 38’ E) is located on the east coast of India adjoining to the Bay of Bengal (Figure 1). This is the largest brackish water coastal ecosystem in Asia and second largest in the world. It is designated as a Ramsar site during 1981. This unique ecosystem is very rich in floral and faunal resources that provides vast support to the socio-economic status of fisher folks through capture fisheries and tourism.

This lagoon has unique assemblage in the four Fig. 1 — Map showing India, Odisha, Chilika lagoon and different ecotones such as northern freshwater sector, specimen observation point (red dot). MAHAPATRO et al.: DISTRIBUTIONAL OF HALIEUTAEA INDICA 1595

the natural disturbances. Consequently, the lake inlet spines four rooted, at the edge of the disk they project was closed and a new natural inlet was dredged to open freely and accompanied by delicate cuticular during 23rd September 2000 4,5. Afterwards, two more processes; the anterior extremity of the roof of the inlets opened naturally thereby providing a suitable tentacular cavity contains a movable luring structure, habitat for the congregation of an array of species. bi-lobed inferiorly and a median lobe located The biodiversity of fishes in Chilika were superiorly at the end of illicium trilobite just above studied well and documented beginning with that of the mouth; mouth horizontal often arched, jaws B.L. Chaudhuri6. Many authors have contributed immovable; blunt teeth in the jaws, palatine and considerably to the faunal study of this lake. The vomerine teeth to crush the hard shell of invertebrate; occurrence of any species belonging to the family eye colour blue, of moderate size, visible in dorsal Ogcocephalidae has not been reported till date,7,8,9,10. view but directed antero-dorsally; width of the eye The present study describes the first record of an about equal to the interorbital space. Upper surface of Ogcocephalid member from Chilika Lagoon with the body bright red in colour, hard, rough and full morphometric and meristic characters have been with macroscopic spines but ventral side white in delineated. colour, very soft and also contained with microscopic spines; few dark red patches found in the ventral side; Materials and methods pectoral fins longer than the pelvic fins, that located On a routine survey in the Outer channel region of much anterior to the pectorals13,14,15,16. Chilika Lagoon, two specimens of unidentified fishes were collected from the shallow intertidal area of Colour Rambharatia region of the lagoon during March 2010. In live, the body colour was bright red to dark red The observed location is situated about seven on the surface and white on the base. In spirit the kilometres inside of the lagoon inlet. The average dorsal surface white, densely covered with very depth of the location “Rambharatia” was 2 (range 1.2 minute black dots, which are grouped together in to 4 metre) and the mean salinity was almost 27 psu places to form thin lines and reticulated patterns. (range 25 to 34 psu). The specimens were collected Ventral surface is white (somewhat translucent) with and preserved in 10% formaldehyde solution and kept scattered minute black and opaque with white dots. in laboratory for proper identification. The species Pectoral fins are colourless, caudal fin clouded with level identification was confirmed by following gray, occasionally with white, vertical bands. Colour relevant literature11,12,13 and FishBase 14. After of dorsal surface of living specimens is pink. After proper identification, the morphometric and meristic preservation the surface showed a combination of dark gray patches with fade white colour, the base characters are recorded and presented in Table 1. 13,14,15,16 The photographic evidences were taken as well as white with black opaque patches . steps are taken to understand the composition of the After analysing all these features, the collected gut content since no information through published specimen is identified as Halieutaea indica Annandale literature found till date. The specimens are with the & Jenkins 1910 (Figure 3 a & b, Table 1). This first author as Ph.D. collections. species is also known as Indian hand fish and this belong to the following taxonomic classification: Results and Discussion Class-

Identification Order- Lophiiformes The observed specimen (Fig. 2, Fig. 3a &b, Family- Ogcocephalidae Gill, 1893 Table 1) has the following morphological features: Genus- Halieutaea Valenciennes, 1837 head is disc shaped dorso-ventrally flattened; with a Species-Halieutaea indica Annandale & Jenkins, conspicuous cavity in front; tail excluding the caudal 1910 (Figure 2, Figure 3a &b) fin; from 1/4 to 1/3 length of disk; caudal fin is longer Feeding habit than the tail; occasionally of the same length; length The feeding habit of Halieutaea indica usually and width of disk measured almost equal; dorsal includes the benthic invertebrates14, but no specific surface covered with numerous strong sub-equal information is available. It’s mouth is specialized to spines; margin of the head region contains trifid crush the hard shells of mollusc and exoskeleton of spines; spines of the tail region bifid and spines over crustaceans since two pair of vomerine teeth are the body surface single but not bifurcated; most of the strategically located upper and lower jaw in such a 1596 INDIAN J. MAR. SCI., VOL. 47, NO. 08, AUGUST 2018

Table 1 — Comparison of morphometric and meristic characters of H. indica from different parts of India and Chilika Lagoon, Bay of Bengal Sl.no. Location Gulf of Kuchh, Chennai Coast Chilika lake Gujrat (Present study) Morphometric and Dash et al., 2013 Silambarasan et al., 2016 Specimen -1 Specimen-2 meristic characters 1 Total length 8.3 7.2 8.3 7.5 2 Dorsal fin length 0.8 0.8 0.8 0.5 3 Pectoral fin length 1.6 1.7 2.6 1.9 4 Pelvic fin length 1.5 1.3 1.3 0.8 5 Anal fin length 1.2 0.8 1.4 0.9 6 Caudal fin length 2 0.7 1.9 1.1 7 Inter orbital space 0.5 0.9 0.7 0.4 8 Eye diameter 0.5 0.5 0.7 0.5 9 Disc length 4.2 5.6 4.5 4.1 10 Disc width 5.5 5.9 5.5 5 11 Tail length 4.1 2.1 4.1 3.4 12 Mouth width 2.3 2.1 2.2 1.4 13 Tentacular cavity 1.6 0.6 width 14 Oral arrangements 11 11 below mouth 15 Width of gill opening 0.5 0.3 16 No. of spines over the 9 9 mouth 17 No. of large spine 5 5 over the mouth 18 Length of the median 0.5 0.3 spine over head 19 Width of luring 0.5 0.3 structure over head 20 Body colour dorsal (in Bright red with dark grey patches Bright red with dark Bright red with dark grey live) grey patches patches 21 Body colour ventral white or translucent with dark grey patches white or translucent white or translucent with dark (in live) with dark grey patches grey patches 22 Dorsal fin spine and 0+4 0+4 0+4 0+4 rays 23 Anal spine and rays 0+4 0+3 0+4 0+4 24 Pectoral fin spine and 0+8 0+7 0+8 0+8 rays 25 Caudal fin rays 8 8 8 manner that it can able to break the shells without inside the illicial cavity secrets some of the chemical more effort. Gibran and Castro 17 & Nagareda18 stimulant that attracts the prey within the attacking reported that some of the members of Ogcocephalidae range from the sediment or a hiding area. This family usually prefer small benthic invertebrates such finding is further supported with the experimental as gastropods, crustaceans, and as prey. observations of Nagareda & Shenker20. They found Certain workers argued that the benthic invertebrates that Polkadot batfish cubifrons secrete could be stimulated by visual stimuli. But, fact is most a chemical attractant due to which a Nassarid of the shallow water benthic organisms live buried in gastropod (Nassarius vibex) is lured and attracted the sediment during day time and active during towards the O. cubifrons. The finding also tells night17,18. Most of the batfishes are active during that the response rate was not 100% all the time by nighttime. Therefore this hypothesis is not accepted O. cubifrons. They20 could able to establish an regarding the use of visual stimuli emerged by batfish indirect relationship between the function of “esca” as to lure benthic invertebrates. However, the work of luring device with the stomach content of Polkadot Bradbury15,16 followed by Combs19 suggests that batfish. In the present study, we tried to understand luring structure (esca) of batfish or hand fish located the components of gut content of H. indica which has MAHAPATRO et al.: DISTRIBUTIONAL OF HALIEUTAEA INDICA 1597

Fig. 3 — Different images of H.indica collected from Chilika lagoon: a. dorsal side, b. Ventral side c. Skeletal system , d. hand like modification of fin, e. Tail region, f, frontal head region: 1&2 blue

coloured eye located antero-dorsally; 3. luring structure the esca; 4&5. Fig. 2 — Image showing first documentation of Halieutaea Indica Immovable upper and lower jaw, g. Different parts of mouth and its (Indian hand fish) by Annandale & Jenkins 1910 collected from accessories: 1. Luring structure, 2&3 vomerine teeth, 4. Gut and offshore region Ganjam coast by Bengal Government’s steam alimentary canal, 5. buccal cavity, 6. Lower pair of vomerine teeth. trawler nammely "Golden Crown" during the year 1908-1909. not been evidenced anywhere from the review of the published literature from India so far.

Gut content analysis The total length of the alimentary canal of the observed species from Chilika lagoon is 5.4 cm (Figure 4a) and 4.9 cm for each of the specimen. Pictorial evidences of the gut content are available in the figure no. 4. The observed gut content of the H. indica exhibited a wide range of feeding preferences, most of the prey belonging to benthic macrofauna community (Figure 4b - 4f), free living nematode (Figure 4g) and filamentous cyanobacteria (Figure 4h). The relative abundance of the same can be viewed from the figure no. 5. It showed crushed carapace of prawn (50 %), crab (40 %), benthic Gammaridea amphipod shared 8 %. They altogether contributed 98 % of the total bulk of the gut followed by nematode and filamentous cyanobacteria having Fig. 4 — a. alimentary canal of H.indica, b. Crushed carapace of crab,c. Chelate leg of crab, d.&e. Crushed exoskeleton of prawn, share of 1 % each. Presence of benthic crustaceans in f. Undigested exoskeletonof benthic Gammaridea amphipod, g. gut of bat fish was already reported in some of the free living nematode, h. Filamentous cyanobacteria 1598 INDIAN J. MAR. SCI., VOL. 47, NO. 08, AUGUST 2018

Fig. 5 — Relative abundance of gut content of H.indica from Chilika lagoon

21 members of ogcocephalidae family . Nagareda & 21 Shenker while working on the temporal variation of Fig. 6 — Images showing the luring structures. a. luring structure the stomach content of three species of batfishes esca of Halieutaea indica, b. Closure view of esca , c.a to c.h . namely Halieutichthys aealeatus, Otocephalus Luring structure of different genus of the family Ogcocephalidae c.a Halieutaea, c.b. Dibranchus, c.c. Ogcocephalus, c.d. declivirostris, and Ogcocephalus pantosticus of Gulf Zalieutes, c.e. Halicmetus, c.f. Malthopsis, c.g. lure of of Mexico observed that the batfishes preferred a Halieutopsis micropus and c.h. lure Halieutopsis vermicularis variety of benthic invertebrate community. According showing structural differences within the same genus. Note: to them, their gut content was composed with Genus Halieutichthys (not shown) resembles Genus Malthopsis in gastropods, worms, and xanthid crabs. having a simple median bulb but delicate dorsal cirri become absent. Genus Coelophrys resembles to Halieutopsis. (Modified Most interestingly, the oral region of the Indian from Bradbury 1967). hand fish is designed to crush the hard shells of molluscs too. But, we did not encountered presence of an indirect relationship of this chemical attractant to any molluscan debris in the gut content. Although, the that of the presence of particular type of food material H.indica prefers benthic mode of life and its prey is such as in the gut content of polkadot bat fish. comprised of sedimentary invertebrates. Nevertheless, A nassarid gastropod Nassarius vibex eventually the amount of sediment in the gut content as observed observed in the gut of polkadot bat fish which is during the present study is negligible. Thus, these two experimentally proved to be lured by the chemical facts leads to an assumption that probably there are stimuli released by esca of the said species20. some extraordinary adaptations involved in the The esca of Indian hand fish as observed during the feeding habit of H.indica . that although, this species present study is shown in the figure 6a and b. As is living within the sediment but can able to avoid revealed in both the figures (Figure 6a and b) esca is engulfing sediment during feeding process. Again, it attached within skull is called the illicial cavity. The is well known that Indian hand fish is a carnivorous esca of Halieutaea indica is fleshy, bi-lobed structure, feeder but not a very efficient swimmer like the tilted forward and downward but connected to the pelagic fishes. Hence, often creeps on the bottom illicium of the skull (Figure 6b) which is highly sediment or jump by using its pectorals. Such developed, prominently visible at the upper region of movement may be good for locomotion but not the mouth. appropriate for the feeding behaviour. Therefore, the The role of esca in capturing of prey is successfully cryptic function of esca (Figure 6 a &b) as the luring explained15-20. The ogcocephalidae family showed device to trap its preferred food from the sediment for much diversification in esca throughout the genus Halieutaea indica becomes significant. (Figure 6c). The Halieutaea indica as evidenced

Role of “esca” in feeding strategy during the present study refers to a very selective kind The esca is also known as the luring device of feeding habit probably by using esca. However, in possesses a bilaterally symmetrical structure which is the present context related to Chilika Lagoon, it need glandular in nature having the pheromone secreting to be verified experimentally before taking the above cells20. It has been proved experimentally that there is mentioned fact into final consideration. MAHAPATRO et al.: DISTRIBUTIONAL OF HALIEUTAEA INDICA 1599

Distribution This study related to first record Halieutaea indica Halieutaea indica is known to have wide distribution provides the first baseline information on this aspect. in the Indo-west Pacific region, from off South Africa, Madagascar, Seychelles, Western Australia, 14 Acknowledgements Philippines, Indonesia, Taiwan, China and Japan . Authors are grateful to the Director, Zoological This fish is also recorded from all along the deeper 11,13,22 Survey of India, Kolkata, Chief Executive, Chilika waters of the east coast of India . Development Authority, Bhubaneswar, Odisha and Head, P.G. Department of Marine Sciences, Remarks Brahmapur University, Odisha, India. One of the The species was first described from off Gopalpur authors RKM also extends thanks to the Director, coast, India13. In recent years this species was NCAOR, Goa for his continuous encouragements reported from Visakhapatnam coast 22, Odisha for the scientific publication. This contribution coast 11,23, the Gulf of Mannar24, off Gujarat coast is a part of the Ph.D. thesis of first author. Authors (depth 80-100 m)25, Kerala coast26 and Chennai are also thankful to the Wold Bank sponsored coast27. All occurrence records of this species are Integrated Coastal Zone Management Project pertaining to deeper seawater, but absolutely there is (ICZMP) under MoEF, Govt. of Odisha for the no report from any brackish water body or shallow financial assistance. coastal regions except the present study.

On the other hand, after opening of the new rd References lagoonal inlets during 23 September 2000 and 1 Nelson, J.S., Fishes of the world (4th ed.). John Wiley & subsequent opening during 2008 the outer channel Sons, Hoboken, USA (2006) 601 pp. area and the Magarmukh region of the lake Chilika is 2 Derouen, V.B.L., William, Ho, Hsuan-Ching and becoming enriched with an array of the benthic Chakrabarty, P., Examining evolutionary relationships and communities such as sponges, cnidarians, molluscs, shifts in depth preferences in batfishes (Lophiiformes: Ogcocephalidae). Molecular Phylogenetics and Evolution, sea hare, polychaetes, amphipod, isopods, prawn, 28-36 84 (2015): 27–33, http://dx.doi.org/10.1016/j.ympev.2014. crab, lobsters, starfishes etc . Since most of the 12.011. fishes, shellfishes and their juvenile depended on 3 Mishra, S.S., Kosygin Singh, L., and Gopi, K.C., FISHES. benthic invertebrate fauna. Thus, Chilika provides an In, State-of-the-Art-Report: Resources of India. ideal feeding ground for a variety of marine faunal Zoological Survey of India, Kolkata. (in press) 4 Mohapatra, A., Mohanty, R.K., Mohanty, S.K., Bhatta, K.S. community to invade the lagoon ecosystem for their and Das, N.R., Fisheries enhancement and biodiversity survival. assessment of fish, prawn and mud crab in Chilika lagoon Present study is significant in three worthy points through hydrological intervention. Wetlands ecology and such as: (i) this is first time ever to record H.indica Management, 15(3) (2007): 229–251. from a shallow brackish water coastal ecosystem i.e. 5 Panda, S., Bhatta K.S., Rath, K.C., Misra, C.R., and Samal, R.N., The Atlas of Chilika, Chilika Development Authority, the Chilika, (ii) gut content analysis of H.indica Bhubaneswar, India (2008) 133 pp. describes the presence of benthic crustacean 6 Chaudhuri, B.L. Fauna of the Chilka lake: Fish (Part I). community (eg. prawn, crabs and amphipod carapace) Memoirs of lndian Museum, 5(4) (1916): 403-440. that shared 98 % of the total bulk and (iii) the role of 7 Mohanty, R.K., Mohanty, S.K., Mohapatra, A., Bhatta, K.S., the luring structure “esca” cannot be ruled out Pattanaik, A.K., Post-ecorestoration impact on fish and shellfish biodiversity in Chilika lake. Indian J. Fish. 53 (4) completely to explain the feeding behaviour of H. (2006): 397–407. indica in Chilika. However, uncertainties still prevail 8 Satapathy, D., and Panda, S., Fish Atlas of Chilika, Chilika to explain the reason of it’s occurrence in Chilika Development Authority, Bhubaneswar (2010): 74 pp. lagoon. It could be due to the increased abundance of 9 Mohapatra, A., Mohanty, S.K. and Mishra, S.S., Fish and macrobenthic communities in the outer channel area Shellfish Fauna of Chilika Lagoon: An Updated Checklist, In: Venkataraman, K and Sivaperuman C. (eds), Marine after opening of the lagoon inlets. Or else it might Faunal Diversity in India , Ecology and have drifted into the lagoon under tidal influence Conservation. Academic Press, Elsevier (2014): 195-222. trough the widened inlets. Since, there is no 10 Mohanty, S.K., Mishra, S.S., Khan M., Mohanty R.K., information on its population dynamics. Therefore, It Mohapatra A. and Pattnaik A.K., Ichthyofaunal diversity of Chilika Lake, Odisha, India: an inventory, assessment of becomes difficult to derive any conclusion within the biodiversity status and comprehensive systematic checklist existing sets of information. More study on this aspect (1916–2014). Check List 11(6) (2015) 1817 (19 pp), doi: is required in future to gather relevant information. http://dx.doi.org/10.15560/11.6.1817. 1600 INDIAN J. MAR. SCI., VOL. 47, NO. 08, AUGUST 2018

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