Description of Panulirus brunneiflagellum new species with notes on its biology, evolution, and fisheries
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1 New Sekiguchi Zealand & George Description Journal of Marine and of Freshwater Panulirus brunneiflagellum Research, 2005, new Vol. species 39: /05/ The Royal Society of New Zealand Description of Panulirus brunneiflagellum new species with notes on its biology, evolution, and fisheries HIDEO SEKIGUCHI Faculty of Bioresources Mie University 1515 Kamihama-cho, Tsu Mie , Japan RAY W. GEORGE Centre of Excellence in Natural Resource Management University of Western Australia Albany WA 6330, Australia Abstract The new species is distinguished from its nearest relatives by the colour and patterning of the anntennual rami. Panulirus brunneiflagellum is morphologically close to P. japonicus and is restricted to the subtropical Ogasawara Islands in the west Pacific. It probably became isolated from the P. japonicus stock with the development of the unique Ogasawara oceanic circulatory system as a result of the deflection of the Kuroshio subgyre as the Iwo-Jima Ridge uplifted. Over 90% of the annual production of c. 5 t is frozen and transported to the Tokyo market, Japan. Keywords Panulirus brunneiflagellum; evolution; new species Panulirus; fishery M04038; Online publication date 8 June 2005 Received 10 February 2004; accepted 2 June 2004 INTRODUCTION A review of the Panulirus japonicus species complex was published by George & Holthuis (1965) in which keys, descriptions, and figures distinguished the geographically restricted species P. japonicus, P. marginatus, P. pascuensis, P. cygnus, and the widespread, and subsequently proven to be confusing, P. longipes (see George 1997 and Chan & Ng 2001, for details of taxa related to P. longipes, and debate over their nomenclature). George & Holthuis (1965) recognised two subspecies of P. longipes, the nominate P. longipes longipes with spotted legs of the Indian Ocean and a striped-legged form (called by them P. longipes femoristriga) inhabiting the western and central Pacific Ocean. George (1972), Sekiguchi (1991), and Chan & Chu (1996) recognised that P. l. femoristriga comprised more than one taxon and, as part of a study of evolution of Panulirus, George (1997) concluded that three taxa, all possessing striped legs, have been identified commonly as P. l. femoristriga. The key distinguishing features allowing separation of these three taxa with striped legs is the coloration and patterning of the antennular flagella. Two of the striped-legged taxa were described and figured by Sekiguchi (1991) who used the local Japanese names at Ogasawara Islands of Aka-ebi (brown whisker) and Shirahige-ebi (white-banded whisker) to distinguish them. Panulirus femoristriga sensus strictu is recognised by the distinctive one white and one darl ramus of each antennule and is known as Shironuke (plain white whisker) by Japanese fishers. According to Chan & Ng (2001) who examined the nomenclature of P. l. femoristriga, P. bispinosus, and P. albiflagellum, Shirahige-ebi is identical to P. l. bispinosus and Shironuke to P. femoristriga sensus strictu (synonym P. albiflagellum). Thus, we believe a new Panulirus name should be given to Aka-ebi. In December 1998, the two authors visited Chichi-Jima in the Ogasawara Islands to gather first hand data. This paper formally describes Aka-ebi as the new taxon and provides notes on its speciation,
2 564 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 habitat, and fishing importance. Measurements are of median carapace length from between the rostral horns and the posterior margin of the carapace. SYSTEMATICS Panulirus brunneiflagellum sp. nov. (Fig. 1, 2A C, 3A) Aka-ebi: Sekiguchi 1991; Chan & Chu 1996 Panulirus aka : George 1997 Material examined Holotype Ogasawara, Mukojima Chain, in trap, November 1997, male, mm (Western Australian Museum, WAM C23504). Paratypes Ogasawa, Mukojima Chain, in trap, November 1997, 1 male, 90.5 mm (WAM C23507), 2 females, 98.4 and mm, with spermatophores (WAM C23505 and C23506). Chichi-Jima, in commercial holding tanks 12 December 1998, 3 females each with spermatophore and 4 males, mm. Description of male holotype Antennular plate with two principal anterior spines and two posteriorly diverging rows of three spinules behind the principal pair of spines; ventral surfaces of distal two segments of antennal peduncle without spinules, distal segment with central pair of major spines, second segment with central pair and basal pair of major spines (Fig. 3A); exopod of third maxilliped with multi-articulate flagellum reaching half length of merus of endopod (Fig. 2C); exopod of second maxilliped with multi-articulate flagellum reaching well beyond endopod (Fig. 2B); posterior margin of thoracic sternum with distinct pair of posteriorly directed teeth; male reproductive opening with curved, raised chitinous ridge without setal tuft; outer margin of triangular plate (plate D) on first abdominal somite with very slight indentation; anterior margin of second abdominal pleura nearly straight with one very minute spinule (Fig. 2A); transverse grooves of second to fourth abdominal somites uninterrupted, very slightly medianly indented; lateral end of second transverse groove does not join pleural groove, lateral end of transverse groove of third somite on right side only, does not join pleural groove, remainder join corresponding grooves; all grooves covered by fringe of setae; apart from setae along posterior margin of the somites and those along the transverse grooves, abdominal terga entirely naked; male pleopods without endopods. Colour Antennule peduncle blackish-purple with white spot at distal articulations and lateral white irregular line; antennular flagella uniformly brownish without crossbands; antennular plate blackish-purple with a large central triangular white spot; antennal peduncle blackish-purple with pale spots and orange tips to dark spines; antennal flagella uniformly dark gray; supraorbital horns blackish-purple with orange tips and large baso-ventral white spot; dorsal carapace blackish-purple anteriorly, brownish centrally and posteriorly, laterally more orange with pale spots, many spines white and orange tipped; continuous mid lateral stripe on carapace, ventral stripe broken and spotted; posterior carapace margin blackishpurple with 13 distinct white spots; cervical groove with fine white spots and stripes; dorsal abdomen blackish-purple with many white and orange dots and laterally, small white spots and larger spots especially on plate D, behind each somite articulation and on abdominal pleura; pereiopods purplish, merus longitudinally streaked with five irregular, narrow white lines; carpus and propodus with dorsal orange stripe, articulations orange; pleopods bordered white with basal spot; telson bordered yellowish. Variations in paratypes In the series examined, the rows of diverging spinules behind the principal pair on the antennular plate ranged from 1 to 5; the exopod of the third maxilliped of the smallest male and in two females reaches only one third of endopod and in another female the exopod reaches only the base of the merus of the endopod; four of the five males have the distinct pair of spines on the thoracic sternum like the holotype, but in one male there is only one very small spinule on the right side; in two females (one with and one without spermatophore) it is reduced to two tiny spinules, and in the remaining mature three females (with spermatophores) the teeth are absent. For two of the four males and for three of the five females in the paratypical series, the transverse groove of the second abdominal somite does not join the pleural groove, for the other two males and one female this transverse groove does join the pleural groove (as is the situation for a specimen described by Sekiguchi (1991) from Hachijo Island), the joining of the transverse groove and pleural groove in the remaining female is very
3 Sekiguchi & George Description of Panulirus brunneiflagellum new species 565 Fig. 1 Panulirus brunneiflagellum. Female with spermatophore from Ogasawara Islands, 120 mm carapace length. A, dorsal view of abdomen; B, lateral view of abdomen; C, lateral view of carapace; D, dorsal view of carapace; E, antennular flagella (after Sekiguchi 1991).
4 566 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 Fig. 2 A C, Panulirus brunneiflagellum. D F, Panulirus longipes bispinosus. A and D, lateral view of abdomen; B and E, second maxilliped; C and F, third maxilliped. Short hairs along transverse and pleural grooves of abdomen and spines of second and third maxillipeds are omitted. Scale = 10 mm for A and D, and 5 mm for B, C, E, and F (after Sekiguchi 1991). indistinct. Thus six of the 10 have the condition as described for the holotype. For the females the small white spots and orange dots on the dorsal and lateral surfaces of the abdomen are larger and provide a more even cover than for the males. Fig. 3 Ventral view of distal two segments of antennal peduncle. A, Panulirus brunneiflagellum holotype male, WAM23504; B, Shirahige-ebi (Panulirus longipes bispinosus). Scale = 10 mm. Distribution Panulirus brunneiflagellum is the dominant species in the southern islands of the Izu Ridge at the Ogasawara Islands (Bonin Is.). These islands are c km south of Tokyo, Japan and 1500 km north of Saipan, Mariana Islands. It has also been recorded from Hachijo Island at the northern end of the Izu Ridge, c. 300 km south of Tokyo (Sekiguchi 1991). Panulirus l. bispinosus (referred to in Sekiguchi 1991 as P. l. femoristriga), the other less abundant taxon from Ogasawara Is., has been recorded from
5 Sekiguchi & George Description of Panulirus brunneiflagellum new species 567 two separate subtropical regions of the west Pacific. It occurs in the north-west Pacific (10 35 N) at the near-asian islands of Japan, Ryukyu Archipelago, Taiwan, and Philippines and the offshore islands of Ogasawara and Hachijo (Sekiguchi 1991). Another population occurs in the south-west Pacific (15 32 S) on the moderate sized islands of Cook, Fiji, Vanuatu, and New Caledonia as well as the mid east coast of Australia (George & Holthuis 1965; George 1972; Sekiguchi 1991; Chan & Chu 1996). Habitat Panulirus brunneiflagellum lives in open caves, down steep volcanic slopes from surface to 90 m in clear oceanic waters. It usually occupies the entrance of the caves, occasionally sharing the cave with P. l. bispinosus, however P. l. bispinosus usually shelters singly or in small groups in the deep recesses at the back of the cave (Nishikiori & Sekiguchi 2000). In the spawning season the two species form separate groups in separate caves. Tides at the Ogasawara are semidiurnal with a spring range of 1.5 m. Currents can run strongly between islands but swells are minimal. Surface water temperatures range from 19 to 29 C. In contrast, habitat records of P. l. bispinosus are as follows: Coral reef (Fiji and Heron Island), speared or netted in shallow water (Japan, Philippines, and New Caledonia) and taken in lobster traps to 130 m (Vanuatu and Australia) (George & Holthuis 1965; George 1972; Juinio et al. 1991). In the Ogasawara Islands, P. l. bispinosus usually shelters singly or in small groups in the deep recesses at the back of the cave (Nishikiori & Sekiguchi 2000). Fishery Nishikiori & Sekiguchi (2001) report that Japanese fishers have taken lobsters ever since the Ogasawara Islands were occupied more than 150 years ago. They are usually caught between 10 and 40 m depths in steel-framed rectangular traps covered with plastic mesh. Each trap measures c. 1 m 0.5 m 0.5 m and has a funnel entrance at each end. The buoyed traps are set singly each day on the volcanic rock slopes, baited with fresh fish. Twenty fishing boats work out from Chichi-Jima Island and two to four boats from Haha-Jima Island, catching an average of c. 5 t annually, 90% of which is frozen and transported to the Tokyo market. P. brunneiflagellum makes up 98% of the catch and the remainder is P. l. bispinosus, except for a few P. penicillatus. The catch was 6 t in 1997 and 9 t in The fishery is regulated by Tokyo Metropolitan Fisheries; a closed season operates from June to August to protect berried females. Species relationships and distinguishing features among the Panulirus japonicus species group Panulirus brunneiflagellum and P. l. bispinosus belong to the P. japonicus group (Group 1 of George & Main 1967) because they possess multi-articulate flagella on the exopod of both the second and third maxillipeds (Fig. 2B,C,E,F). Like all Indo-West Pacific Group 1 they also have uninterrupted dorsal transverse grooves across the abdominal segments and have one major pair of spines on the antennular plate thus separating them from the East Pacific P. interruptus and the West Atlantic P. argus which have medianly interrupted abdominal transverse grooves and two pairs of major spines on the antennular plate. Panulirus brunneiflagellum is distinguished from P. marginatus, P. cygnus, and P. femoristriga in having the transverse groove on the second abdominal segment not joining the corresponding pleural groove, whereas the grooves on all abdominal segments join the corresponding pleural grooves in these other species. In this character P. brunneiflagellum is closest to P. japonicus and P. pascuensis. However, P. japonicus also has the third and fourth abdominal transverse grooves not joining the pleural grooves and the males of P. japonicus are unique in usually having simple or bifid endopods of the pleopods of the second to fifth abdominal segments (George & Carlberg 1995). In P. brunneiflagellum, antennular flagella are plain and the abdomen spotted whereas in P. pascuensis antennular flagella are banded and pale bands are present on the abdomen. The two subspecies of P. longipes, P. l. longipes and P. l. bispinosus, together with P. femoristriga form a close group sharing the basic morphological characteristics of Group 1 multiarticulate flagella on the endopods of the second and third maxillipeds (Fig. 2E,F), medially uninterrupted absomenal transverse grooves that all join laterally with the pleural grooves (Fig. 2D) and one pair of major spines on the antennular plate. In the past, positive identification of preserved specimens was often very difficult when colour patterns had been obliterated or modified. The colours of fresh material make positive identification possible by combinations of patterns. P. l. longipes and P. l. bispinosus have banded antennal and antennular flagella (Fig. 4E), a distinct bow mark behind the cervical groove, and a single pale stripe along the lateral carapace (Fig.
6 568 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 Fig. 4 Shirahige-ebi (Panulirus longipes bispinosus). Male from Ogasawara Islands, 145 mm carapace length. A, dorsal view of abdomen; B, lateral view of abdomen; C, lateral view of carapace; D, dorsal view of carapace; E, antennular flagella (after Sekiguchi 1991).
7 Sekiguchi & George Description of Panulirus brunneiflagellum new species 569 4C,D); they are distinguished by the broad pale stripe along the legs of P. l. bispinosus and the broad pale stripe broken by three white spots along the legs of P. l. longipes. P. femoristriga has plain (one white, one dark ramus) antennular flagella, a wishbone mark behind the cervical groove, two pale stripes along the lateral carapace, and narrow white stripes along the legs. As mentioned above, P. brunneiflagellum is morphologically close to P. japonicus. However, as part of his study of the phyllosoma larvae of all the species in the P. japonicus group that occur in the Kuroshio subgyre, Dr T. Yoshimura (pers. comm.) used the Internet web DNA database for identification and concluded that P. brunneiflagellum has the closest genetic affinity with P. femoristriga. It is not apparent at this time whether the morphological or the molecular data provide a better appraisal of the true relationships of P. brunneiflagellum. P. japonicus have ever been recorded there and that only a few larvae of P. l. bispinosus and even fewer larvae of P. penicillatus settle from the nearby west Philippine Basin suggest that a discreet current system circulates around the volcanic island chain (Sekiguchi 1991). This current system probably developed from a major deflection of the Kuroshio subgyre by the elevation of the Iwo Jima Ridge and it is now responsible for the transport and circulation of P. brunneiflagellum phyllosoma larvae away from and back to the Ogasawara Islands. Although the Ogasawara Islands may have become subaerial only c. 2 Ma, a significant deflection of the oceanic currents and the subsequent genetic separation of P. brunneiflagellum may have been possible at an earlier time since both P. brunneiflagellum and P. japonicus would be capable of living on any of the ridges or seamounts as they gradually came closer to the surface at depths of at least 90 m. SPECIATION When suggesting possible evolutionary processes to explain the isolation of P. brunneiflagellum, volcanic ridge uprisings in the north-west Pacific are important events contributing to their subsequent geographic separation. According to Kennet (1982), from late Oligocene (30 Ma) a major pulse of volcanism occurred near the continental margin of Japan, peaking about middle Miocene (12 Ma) and this was followed in late Miocene (9 Ma) by a dramatic cold water upwelling and increased oceanic turnover, indicated by the high productivity and altered composition of diatoms. It was into this environment that P. japonicus evolved as it moved north from its equatorial origin which it had shared with the incipient P. cygnus, and it biologically responded to the Kuroshio subgyre which is the dominant oceanic current system of the region (Sekiguchi 1991). According to Springer (1982), in the middle Miocene a period of volcanism along the Palau- Kyushu Ridge resulted in the formation of the eastward moving West Mariana Ridge. Sundering along the West Mariana Ridge c. 5 Ma years ago formed the Mariana Trough and produced the volcanically active Mariana Island Ridge to the east. The Iwo Jima Ridge which contains the Ogasawara Islands is a Pliocene (2 Ma) volcanic extension of this Mariana Trench system. The fact that P. brunneiflagellum is the clearly dominant species of Panulirus around the Ogasawara Islands, that no ACKNOWLEDGMENTS We are grateful to Mr K. Nishikiori, Ogasawara Branch of Tokyo Meteropolitan Fisheries Laboratory for helping collecting Aka-ebi specimens at Ogasawara Islands. Thanks to anonymous referees for their comments on the early version of the manuscript. REFERENCES Chan, T. Y.; Chu, K. H. 1996: On the different forms of Panulirus longipes femoristriga (von Martens, 1872) (Crustacea: Decapoda: Palinuridae) with a description of a new species. Journal of Natural History 30: Chan, T. Y.; Ng, P. K. L. 2001: On the nomenclature of the commercially important spiny lobsters Panulirus longipes femoristriga (Von Martens, 1872), P. bispinosus Borradaile, 1899, and P. albiflagelum Chan & Chu 1996 (Decapoda, Palinuridae). Crustaceana 74: George, R. W. 1972: South Pacific islands rock lobster resources. Report prepared for the South Pacific Development Agency. Document WS/C7959. Rome, Food and Agriculture Organisation of the United Nations. 42 p. George, R. W. 1997: Tectonic plate movements and the evolution of Jasus and Panulirus spiny lobsters (Palinuridae). Marine and Freshwater Research 48: George, R. W.; Carlberg, K. 1995: Variation in the male pleopods of Panulirus japonicus (von Siebold, 1824). Crustaceana 68:
8 570 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 George, R. W.; Holthuis, L. B. 1965: A revision of the Indo-West Pacific spiny lobsters of the Panulirus japonicus group. Zoologische Verhandendellingen 72: George, R. W.; Main, A. R. 1967: The evolution of spiny lobsters (Palinuridae): a study of evolution in the marine environment. Evolution 21: Juinio, A. R.; Macaranas, J. M.; Gomez, E. D. 1991: Sympatric occurrence of two subspecies of Panulirus longipes Milne Edwards, 1868 (Decapoda, Palinuridae) and biochemical evidence of interbreeding. Memoirs of Queensland Museum 31: 209. Kennet, J. P. 1982: Marine geology. Englewood Cliffs, New Jersey, Prentice-Hall. 813 p. Nishikiori, K.; Sekiguchi, H. 2001: Spiny lobster fishery in Ogasawara (Bonin) Islands, Japan. Bulletin of Japanese Society of Fisheries Oceanography 65: (In Japanese.) Sekiguchi, H. 1991: Two forms of Panulirus longipes femoristriga (Crustacea: Palinuridae) from Ogasawara waters, Japan. Proceedings of Japanese Society of Systematic Zoology 44: Springer, V. G. 1982: Pacific plate biogeography with special reference to shorefishes. Smithsonian Contributions to Zoology 367:
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