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Iranian Journal of Fisheries Sciences 16(3) 1114-1122 2017

First report of cyclopoid () from north- eastern Arabian Sea, Karachi, Pakistan

Ara M.1; Farooq S.2*; Rabbaniha M.3; Ali Muhammad A.1, 4

Received: March 2017 Accepted: April 2017

1-Center of Excellence in Marine Biology, University of Karachi-75270, Karachi, Pakistan. 2-Marine Science Division, Department of Zoology, University of Karachi-75270, Karachi, Pakistan. 3-Iranian Fisheries Science Research Institute (IFSRI), Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran. 4-Coastal Development and Fisheries Department, Government of Balochistan. *Corresponding author's Email: [email protected]

Keywords: Zooplanktons, Copepods, Cyclopoids, Oithona, Arabian Sea, Mangrove forests, Pakistan

Introduction 54 species of Oithona were recorded Among marine communities, the from the world and 27 species were importance of small species has been reported to occur in the Indian Ocean neglected and major attention has been (Razouls, et al., 2005-2016). The paid to the larger representatives species belonging to genus Oithona (Mazzochi and Paffenhoper, 1998). were reported widely from many parts Small copepods are now assigned as a of Western Indian Ocean including the significant component within marine Arabian Sea (Kasturirangan, 1963; food webs (Tuner, 2004). Their Madhupratap et al., 1992; Al-Yamani et ecological habitat comprises estuarine, al., 2011). They were reported to be the pelagic and coastal environments. most abundant species in the Oithona plays a vital role as a food zooplankton samples. However, in source for other copepods, Pakistan the of copepods Chaetognaths, fish larvae and were mostly confined to the calanoid planktivorous fishes. copepods and the information about the Members of the genus Oithona are diversity of this important and abundant distributed throughout the world genus was limited only to the report of (Nishida, 1985; McKinnon, 2000; single species Oithona plumifera (Haq Galliene and Robins, 2001). More than et al., 1973). Therefore, the present 1115 Ara et al., First report of cyclopoid copepods (oithonidae) from north-eastern Arabian Sea … study was conducted to determine the Results and discussion species composition of the genus Systematics Oithona previously not known from the Family: Oithonidae Dana, 1852 coastal waters of Pakistan. Genus: Oithona Baird, 1843 Diagnosis Material and methods Prosome short, 5 segmented, oval to The zooplankton sampling was fusiform in dorsal view. Anterior conducted monthly (March 2010- margin of cephalosome rounded or with September 2013) at four stations in 1 rostrum in females and truncate Manora Channel and the Sandspit without rostrum in males. Posterior backwater mangrove forest area using margin of cephalosome wide. Posterior zooplankton net (mesh size 170 µm). margin of prosome rounded. First Samples were preserved immediately in antennae twice geniculate in males and 4 % formalin. Cyclopoid copepods of not geniculate in females. P5 with 2 genus Oithona were sorted out from lateral process on pedigerous segment. samples under a stereomicroscope and Urosome slender with 6 somites in examined under a compound males while 5 in females. Genital microscope (using objective lens 100x, somite long and swollen laterally in oil immersion). The total length females, simply cylindrical in males. (measured dorsally from tip of the Caudal rami with 1 outer, 1 dorsal and prosome to the end of the caudal ramus, 4 apical setae (Baird, 1843). excluding caudal setae), prosome length (from tip of head to last thoracic Oithona rigida (Giesbrecht, 1896) segment), urosome length (from last Female size: 0.831 mm (Fig. 1) thoracic segment to caudal rami) of Synonym: Dioithona rigida specimens were measured with a Description calibrated ocular micrometer. Species Cephalosome robust with blunt rounded were identified according to an and anteroventrally bent into blunt identification guide for Oithona rostrum. Prosome short oval, posterior (Nishida, 1985; Razouls et al. 2005). In end with greatest width (Fig. 1a). the text the following abbreviations are Prosomal length is 0.44 mm. Posterior used: mandibles (Md), maxillule width of cephalosome is 0.2 mm and (Mx1), inner lobe 2 of maxillule (Li2); urosome is 0.43 mm. A1 0.8 times of outer lobe 1 of maxillule (Le1), maxilla prosomal length. A2 base bears 3 setae; (Mx2), antenna (A2), antennule (A1) endoode sgment I bears 5 setae 2 and swimming legs (P1 to P5). medial and 3 terminal; endopod segment II 7 termial setae (Fig. 1b). Md basis bears 2 sharp spines, endopod of Md armed with five spines outer most is hirsute (Fig. 1c), whereas exopod 4 segmented with 1, 1, 1, 2 Iranian Journal of Fisheries Sciences 16(3) 2017 1116

setae as in O. oculata. Mx1 endopodite wide. A2 base bears 3 setae covered with 2 setae (Fig. 1d). Terminal with hairs, endopod segment I with 5 modified spine of P4 exopod is equal to setae: 1 medial and 4 terminal, endopod the last segment of the exopod. Caudal segment II armed with 7 terminal setae. rami 3.3 times longer than wide. Outer (Fig. 1g). Mx1 endopodite with 4 setae spines on the exopod of P1 to P4 is 113, with asymmetric size (Fig. 1h). Md 113, 113, and 112. (Fig. 1e). basis comprises of 2 sharp, hirsute and pointed spines. The endopod of Md Oithona oculata (Farran, 1913) ♀ composed of 5 setae 2 proximal and 3 Female size: 0.77mm (Fig. 1 f- l) distally present, exopod is 4 segmented Synonym: Dioithona occulata with 1,1,1,2 setae (Fig. 1i). Terminal Description spines of exopod of swimming legs P1 Cephalosome robust with blunt rounded to P4 is longer than last segment of and anteroventrally bent into blunt exopod. (Figs. 1j and k). P5 consists of rostrum. Prosome short oval, posterior two segments: a broad basal segment end with greatest width (Fig. 1f). O. with long outer seta and a narrow oculata shows resemblance with O. segment with 2 setae; leg present rigida. Caudal rami 2 times longer than laterally on genital somites (Fig. 1 l).

Figure 1: Oithona rigida ♀ (a) dorsal view; (b) A2; (c) Md; (d) Mx1; (e) P IV. Oithona occulata ♀; (f) dorsal view; (g) A2; (h) Mx1; (i) Md; (j) P I; (k) P III; (l) P V. 1117 Ara et al., First report of cyclopoid copepods (oithonidae) from north-eastern Arabian Sea …

Oithona brevicornis (Giesbrecht, 1891) prosomal length. Urosomal somites ♀, ♂ varies in length, divided into 5 somites Female size: 0.69 mm (Fig. 2 a - f) (Fig. 2h). A2 is 5 segmented, basipod Description segment II covered with 1 outer and 1 Prosome elongate and 2 times width of inner seta present at distal end; cephalosome, anteriorly rounded, head Endopod segment II bears 2 outer setae ventrally sharp pointed in lateral view. apart from each other; Exopod segment First antennae reaches up to 2nd III roofed with 7 terminal setae (Fig. metasomal segment only, caudal rami 2i). Md basis bearing 2 sharp curved consist of 4 apical plumose setae and 1 and pointed spines covered with lateral naked setae (Fig. 2a). A2 base spinules. One minute and 3 subequal put up with 3 setae covered with hairs, setae present on endopod, outer most 1 is at inner margin and 2 at outer one is hirsute, exopod 4 segmented with margin while endopod segment I is 1,1,1,2 setae (Fig. 2j). MxI with armed with 5 setae (one proximal, one endopodite one seta which is absent in distal and three terminal) (Fig. 2b); O. fallax which resembles to O. similis. Segment II of endopod bears 7 terminal (Fig. 2k). Terminal spines of P1 to P4 setae. Base of Md bear curved, blunt are 3.5 times longer than the last thick spines; endopod of mandible bear exopod segment (Figs. 2 l and m). P5 of 4 setae outer most is hirsute (Fig. 2c). O. similis with 2 setae present on broad Endopod of Mx1with three setae (Fig. basal segment (Fig. 2n). 2d). P1 exopod III segment has 1 elongated spine with hirsute tip (Fig. 2e). P4 endopod III segment is bearing modified spine (Fig. 2f).

Oithona similis (Claus, 1866) ♀ Synonym: O. helgolandica (Claus, 1863) Female size: 0.744 mm (Fig. 2g - n) Description Prosome elliptical, rounded and long 0.47mm. Antennules slightly longer than prosome about 1.1 times of Prosome. Rostrum rounded dorsally and pointed ventrally (Fig. 2g). The length of prosome is 0.5 mm and 2.6 times to its width in our samples. First antennae reaches up to the end of metasome. Antennule 1 is 0.75 times of Iranian Journal of Fisheries Sciences 16(3) 2017 1118

Figure 2: Oithona brevicornis ♀ (a) dorsal view; (b) A2; (c) Md; (d) Mx1; (e) P I; (f) endopod of P IV with modified spine. Oithona similis ♀ (g) dorsal view; (h) genital somite; (i) A2; (j) Md; (k) Mx1; (l) P II; (m) P IV; (n) P V.

Oithona pseudofrigida (Rosendorn, proximal one large hirsute. Exopod 4 1917) ♀ segmented with 1, 1, 1, 2 setae (Fig. Female size: 0.82 mm (Fig. 3a-g) 3d). Mx1 is shown in figure with one Description setae on endopodite segment (Fig. 3e). Prosome pointed anteriorly elipitical in All swimming legs are diverse, exopod shape; rostrum Antero ventrally pointed of leg I to IV with 3.7-4 times larger and sharp, Urosome with 5 somites terminal spine than the last exopod with three spines on last segment in a segment. Short inner seta present inner lateral view (Fig. 3a and b). A2 basipod margin of exopod I of P2 and P4 (Fig. 3 bearing 3 setae, 2 outer medial and f and g). P3 is characterized with 2 proximal hirsute. Endopod I segment rudimentary spinules on III segment of has 5 setae (1 medial, 1 proximal and 3 exopod. terminal) while second segment has 6 terminal setae, 2 small and naked and Oithona attenuata (Farran 1913) ♀ other 4 hirsute (Fig. 3c). Md basis Female size: 0.68mm (Fig. 3 h-m) occupy 2 sharp, recurved and pointed Description spines covered with hairs; endopod Prosome rounded and increases in possess 4 setae, 3 subequal and width towards posterior end. Lateral 1119 Ara et al., First report of cyclopoid copepods (oithonidae) from north-eastern Arabian Sea … view of species shows small process equal) setae. Md basis has 2 spines one (Figs. 3 h and i). Urosome is slender, small, pointed and sharp and second comprises of 5 urosomal somites. one is thick, pointed, hirsute and Genital segment is 1.4 times longer recovered; endopod with 4 semi equal than wide. A2 basipod segment I bears setae (Fig.3j). Mx1 endopodite 2 inner and 1 outer marginal setae, 1 of constitute 4 setae of subequal sizes and the inner one is hirsute and present at one thick and one thin terminal spine. the base of basipod segment II. 2 setae (Fig. 3k). Terminal spine of exopod of (1 small and 1 large) medially present swimming legs P1 is 3 times longer on second basipod segment. Endopod (Fig. 3 l). P2 to P3 1.5 to 1.7 times of Segment I with 5 setae; 1 medial, 1 longer than last segment of exopod distal and 3 (2 hirsute) terminal setae. (Fig. 3 m). Second endopod segment is terminally covered with 7 (2 small and 5 sub

Figure 3: Oithona pseudofrigida ♀ (a) lateral view; (b) dorsal habitus; (c) A2 (d) Md (e) Mx1 (f) P I (g) P IV. Oithona attenuata ♀ (h, i) lateral and dorsal view; (j) Md; (k) Mx1; (l) P1; (m) P III.

Iranian Journal of Fisheries Sciences 16(3) 2017 1120

Remarks aruensis and O. davisae. The second The present specimens of O. rigida basal segment bears two blunt, thick agree with Nishida (1985) and disagree and slightly curved spines with fine with Giesbrecht (1896). Only slight size spines on margins which are specific to variation was observed in our the Md of O. brevicornis as compared specimens. O. oculata is closely related to the other two species which do not to the O. rigida, differing it by having have blunt and thick spines. large terminal spines of swimming legs O. similis is allied with two species whereas in O. rigida the terminal spines O. fallax and O. decipiens. Our of exopod is shorter than the last specimen of O. similis do not have setae segments of swimming legs. Endopod on the inner margin of the first joint of of MX1 with 2 seate in O. rigida, and 4 P2 to P4, which is the characteristic of setae in O. oculata. O. fallax. MX1 of O. smilis have 1 seta Typical form of O. brevicornis is on Li2 and Le1 with 1 seta which are slightly elongated reported from absent in O. fallax whereas in O. Australian waters and China Sea. The decipens Le1 with 1 seta and Li2 specimen from the Black Sea is slightly without setae. smaller in size (0.5- 0.6 mm♀, 0.45 mm Typical form of O. attenuata is ♂) as compared to our specimen larger in size (0.7-0.8 mm) and the (Selifonova, 2009). The O. brevicornis present specimen is closest to that collected from Pakistani waters have reported by Nishida (1985) and Cleve resemblance with the specimens of the (1901). O. attenuate show similar Persian Gulf as the lateral setae reach characteristics with O. fallax Li1 of beyond the caudal rami unlike the MX1 armed with distal seta twice Australian one in which lateral setae are longer than other setae. All setae on Li1 short. Thus the present specimen of O. are of similar length in O. nana. brevicornis collected from Pakistani O. pseudofrigida closely resembles waters are closest to the ones reported O. frigida, and is distinguished by by Giesbrecht (1891). O. brevicornis having 1 inner marginal setae P1 to P4 share some characteristics with O. segment. Exopod segment 3 of P3 to aruensis and O. davisae. O. brevicornis P4 with short outer marginal spines. 2 differs from these two species in spinules on the exopod third segment of possessing a distal spine on the inner P3 (Nishida, 1985). lobe of Mx1 which is shorter as Research and studies on marine compared to the other two species. In zooplankton species composition was O. brevicornis the inner lobe of MX1 neglected since many years in Pakistan. bears 1 setae like in O. aruensis and no This is the first study on the Oithona setae in O. davisae. Endopod of Md species composition in Pakistani waters with four spines in O. brevicornis after 4 decades. We compared our shares the characteristics of Md with O. specimens with published works from 1121 Ara et al., First report of cyclopoid copepods (oithonidae) from north-eastern Arabian Sea … neighboring countries and other parts of References the world to minimize error in Al-Yamani, F.Y., Skryabin, V., identification. The collections were Gubanova, A., Khvorov, A. and organized in 2010, 2012 and during Prusova, I., 2011. Marine 2013 for the statement that our selected zooplankton practical guide for the species were not introduced artificially northwestern Arabian Gulf. Volume and by ballast water. All of the six 2. Kuwait Institute for Scientific recorded species are permanent Research, Kuwait. 96-102 pp. residents of Pakistani waters. Baird, W., 1843. Notes on British The species composition of Oithona Entomostraca. The Zoologist was reported from many parts of the (Newman), 1,193-197. Indian Ocean (Kasturirangan, 1963). O. Convay, D.V.P., White, R.G., rigida has been reported from Iranian Hugues-Dit-Clies, J., Gallienne, and Indian waters (Santhanam and C.P. and Robins, D.B., 2003. Guide Perumal, 2003). O. brevicornis and O. to the coastal and surface attenuata are reported from India zooplankton of the south- western (Thompson, 1986), Kuwait and Oman Indian Ocean. Occasional (Al-Yamani et al., 2011). O. similis is a Publication of the Marine Biological widely reported species (Nishida, 1985; Association of the United Kingdom, Thompson, 1986). O. spinirostris is No. 15, Plymouth, UK. reported from both Indian and Iranian Gallienne, C.P. and Robins, D.B., waters (Santhanam and Perumal, 2003). 2001. Is Oithona the most important In the present study O. pseudofrigida in the world’s Oceans? was reported for the first time from Journal of Research, 23, north-western Indian Ocean. This 1421-1432. species was reported earlier to occur in Giesbrecht, W., 1896. Uber pelagische the south-western Indian Ocean copepoden des meeres, gesammelt (Convey et al., 2003). The presently vom Marine stabsarzt Dr. Augustin reported species were abundantly Kramer. Zoologische Jahrbücher. distributed in our coastal and mangrove Abteilung für Systematik, forest channel waters and represent a Geographie und Biologie der Tiere, very important component of 9, 315-328. zooplankton samples. Further studies Giesbrecht, W., 1891. Elenco dei are required to ascertain the species copeodi pelageci racolti dal tenente abundance of genus Oithona in other di vascello Gaetano Chierchia near shore waters of Pakistan. durante il viago della R. Corvetta “Vettor Pisani” negli anni 1882- Acknowledgement 1885, e dal tenente di vascello The authors would like to pay gratitude Francesco Orsini nel Mar Rosso, nel to Dr. Shuhi Nishida for her valuable 1884. Att Accad. Naz. Lincei Rc., 4, comments. 7, 474-481. Iranian Journal of Fisheries Sciences 16(3) 2017 1122

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