Vertical Distributions of Phyllosoma Larvae of Palinurid and Scyllarid Lobsters in the Western North Pacific
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1 Journal of Oceanography, Vol. 57, pp. 743 to 748, 2001 Short Contribution Vertical Distributions of Phyllosoma Larvae of Palinurid and Scyllarid Lobsters in the Western North Pacific HIDEKI MINAMI, NARIAKI INOUE and HIDEO SEKIGUCHI* Faculty of Bioresources, Mie University, 1515 Kamihama-cho, Tsu, Mie , Japan (Received 2 May 2001; in revised form 9 August 2001; accepted 10 August 2001) Vertical distributions of phyllosoma larvae were examined in waters east of the Philippines or west of the Mariana Islands (18 56 N to N; E to E) based on zooplankton samples collected with an Isaacs-Kidd Midwater Trawl on September 22 24, Phyllosoma larvae belonged to the two families Scyllaridae and Palinuridae comprising 4 genera and 9 species. Of the collected phyllosoma larvae, those of Scyllarus cultrifer and Panulirus longipes were most abundant and showed similar vertical distributions: (1) both species were collected from the mixed layer at night but not in the day, (2) their vertical distributions did not change with their stages, and (3) the upper limit of their vertical distributions during the day accorded with the base of mixed layer. Furthermore, their vertical distributions were similar to those of lepthocephalus larvae which were collected using the same sampling stations and gear in the present study. Vertical distributions of phyllosoma larvae were discussed in relation to their horizontal distributions. Keywords: Phyllosoma larvae, vertical distribution, diel migration, Western North Pacific. 1. Introduction Phyllosoma larvae have a unique shape and a transparent body and are confined to palinurid and scyllarid lobsters. They metamorphose into puerulus (palinurid) and nisto (scyllarid) larvae, and settle on the sea bottom in their adult habitat areas (Cobb and Phillips, 1980). Palinurid lobsters have a long planktonic life of over 6 months (Booth and Phillips, 1994) while scyllarids have a shorter planktonic life of 2 or 3 months (Robertson, 1968; Ito and Lucas, 1990). However, information is limited on larval recruitment processes vital for clarifying the population dynamics of most palinurid and scyllarid lobsters in the world (Sekiguchi, 1986a, 1997; Inoue and Sekiguchi, 2001), though Phillips and his colleagues published a series of papers dealing with those of Panulirus cygnus in western Australian waters (see Cobb, 1997). Several studies dealing with planktonic larvae dispersing into offshore waters and then returning to onshore waters have deduced vertical distributions and diel migrations of the larval change in relation to their stages and related these with the directions and strengths of currents (e.g. Roughgarden et al., 1988; Sekiguchi, 1997). * Corresponding author. sekiguch@bio.mie-u.ac.jp Copyright The Oceanographic Society of Japan. We have poor information on the mechanisms by which phyllosoma larvae may disperse into oceanic waters and then return to coastal waters where benthic populations of the lobsters are found. In the case of P. cygnus, their vertical distributions and diel migrations change depending on their stages and related to different directions and strength of currents in relation to depths, thus playing an important role in the larval dispersion into oceanic waters and return to coastal waters (Rimmer and Phillips, 1979; Phillips et al., 1981; Pearce and Phillips, 1993). Unfortunately, there is little information on the vertical distributions and diel migrations of phyllosoma larvae except for the publications by Austin (1972) for the Gulf of Mexico, Rimmer and Phillips (1979) for western Australian waters and Yeung and McGowan (1991) for Florida waters. Leptocephalus larvae of the Japanese eel Anguilla japonica, with a long planktonic life of nearly 100 days after spawning in the Mariana waters of the western North Pacific, are transported through the Subtropical Gyre into Japan and its neighboring waters where they metamorphose into glass eels (Tsukamoto, 1992). We assume that both the leptocephalus and phyllosoma larvae, with a long planktonic life, would have similar problems for their larval recruitment processes. Zooplankton samples dealt with in the present study were originally collected to examine 743
2 vertical distributions and diel migration of leptocephalus larvae of the above eel in Mariana waters (Kajihara et al., 1988). 2. Materials and Methods Zooplankton sampling was undertaken on September 22 24, Samples were collected within a small area from N to N and from E to E, east of Luzon Island of the Philippines or west of Mariana Islands (Fig. 1). The North Equatorial Current and Subtropical Countercurrent exist along 15 N and 20 N, respectively. The former current approaches the eastern coast of the Philippines and then separates into two branches of northward and southward flows. The northward flow contributes to generating the Kuroshio Current while the southward flow goes to generate the Mindanao Current (Fig. 1). Using a 3 m Isaacs-Kidd Midwater Trawl (IKMT) with 0.5 mm mesh-openings, zooplankton samples were collected at 7 discrete depth layers (10, 20, 50, 80, 130, 200 and 400 m deep) each by day and night. In order to avoid contamination in lowering and retrieving the IKMT and to filter an equal volume of water in each depth layer, the IKMT with no opening-closing device was towed horizontally for 40 minutes at each depth layer at a ship speed of 2.0 kt (1 m/sec.), following a drifting radar buoy throughout the sampling to filter the same water mass. Sampling depths of the IKMT were estimated using an inclinometer and the length of wire reeled out. Lowering and retrieving the IKMT was done as follows: wire was paid out at 1 m/sec while the ship speed was kept at 2 kt until the IKMT reached each depth layer; the IKMT was towed horizontally at each depth layer for 40 minutes with a ship speed of 2 kt, and then the wire was retrieved at 1 m/sec while the ship speed was kept at 2 kt. This indicates that contamination may not be neglected in retrieving IKMT. It took nearly 1 5, and 20 minutes to retrieve the IKMT from 10 80, and 400 m depth layers, respectively, so that contamination may not be neglected in retrieving the IKMT from 400 m depth layer. However, this contamination may be neglected in the present study because phyllosoma specimens collected at the 400 m depth layer were much more meager in number than those collected at the other depth layers, as mentioned in the results section. Vertical profiles of water temperature, salinity and dissolved oxygen content were monitored at 1 m intervals from the surface down to 1000 m using a CTDO profiler (Neil Brown Mark III). Zooplankton samples were fixed immediately in 10% buffered formalin seawater on board. All specimens of phyllosoma larvae were sorted out in the laboratory. Late stage phyllosoma larvae were identified to the species level according to Sekiguchi (1986b) and Inoue et al. (2000, 2001), while early to mid- Fig. 1. Sampling station (pentagram) and ocean current system in the western North Pacific. dle stages were identified based on their morphological similarity to the late stage ones. Most of the phyllosoma larvae collected in the present study belonged to the genera Panulirus and Scyllarus, so stages of Panulirus and Scyllarus phyllosoma larvae were determined according to Braine et al. (1979) and Phillips and McWilliam (1986). 3. Results 3.1 Species composition A total of 114 phyllosoma larvae were collected. These larvae are referred to two families Palinuridae and Scyllaridae (Table 1). Four species belonged to the two genera (Scyllarus and Scyllarus) of the Scyllaridae and five species to the two genera (Panulirus and Justitia) of the Palinuridae. These include 61 specimens of Scyllarus (S. cultrifer, S. martensii and Scyllarus sp.d), 1 specimen of Scyllarus (Scyllarus sp.), 50 specimens of Panulirus (P. longipes, P. penicillatus, P. ornatus and P. vesicolor), and 2 specimens of Justitia (J. japonica) (Table 1). The two sibling species, P. japonicus and P. longipes, have been classified in the Panulirus japonicus group (George and Main, 1967). It is difficult to distinguish phyllosoma larvae of P. longipes from those of P. japonicus based on morphological features (Inoue and Sekiguchi, 2001). However, we assumed that 40 specimens of the above 50 Panulirus phyllosoma larvae, which were collected in late September, would belong to P. longipes, since the final stage of phyllosoma larvae of P. longipes metamorphoses to the puerulus in October and later, and pueruli settle in October to April (Tanaka et al., 744 H. Minami et al.
3 Table 1. Data for phyllosoma larvae collected in the present study. Species Stage Body length (mm) Number Panulirus longipes VI VII VIII P. penicillatus VII VIII 23.7, P. ornatus VII VIII P. versicolor VII VIII 17.2, Justitia japonica VIII IX Scyllarus cultrifer IV V VI S. martensii VII VIII Scyllarus sp.d VIII Scyllarides sp. V ; Inoue and Sekiguchi, 2001) while the final stage ones of P. japonicus metamorphoses to the pueruli in June to August (Yoshimura et al., 1999), and the puerulli settle in summer (Kanamori and Kanamaru, 1980; Kanamori, 1982). Most of the Panulirus and Scyllarus larvae collected in the present study belonged to P. longipes and S. cultrifer, respectively (Table 1). The 40 specimens of P. longipes consisted of seven specimens in stage VI (BL mm), 22 in stage VII (BL mm) and 11 in stage VIII (subfinal stage, BL mm), while the 57 specimens of S. cultrifer consisted of four specimens in stage IV (BL mm), 50 in stage V (BL mm), and three in stage VI (BL mm) (Table 1). 3.2 Vertical distribution Based on vertical profiles of water temperature and salinity (Fig. 2), the water in the upper m was well mixed with water temperature and salinity of 26 to 28 C and ca psu, respectively. Below the mixed layer water temperature decreased markedly to form a permanent thermocline at least to 500 m depth, while salinity increased to form a maximum at about 150 m depth. We deal here with vertical distributions of phyllosoma larvae of P. longipes and S. cultrifer because these two species were most abundant among the larvae collected in the present study (Table 1). For P. longipes, a total of 25 specimens were collected in the day and 15 specimens at night (Table 2, Fig. 3). Most larvae of P. longipes (21 specimens) were collected at the 80 m depth Fig. 2. Vertical profiles of water temperature, salinity and the dissolved oxygen content within a small area with N to N; E to E. during the day, but were not collected in the upper 50 m while they were collected at 10, 20, 50, 130 and 400 m depths at night (Fig. 3, Table 2). For S. cultrifer, a total of 49 specimens were collected in the day and eight specimens at night. Most larvae of S. cultrifer (44 specimens) were collected at the 80 m depth in the day, but were not collected in the upper 50 m, while they were collected at 10 and 50 m depths at night (Fig. 3, Table 2). Vertical distributions of P. longipes larvae were similar to those of S. cultrifer as follows (Fig. 3): (1) they were collected from the mixed layer at night but not during the day, (2) their vertical distributions did not change with their stages, and (3) the upper limit of their daytime vertical distributions accorded with the base of mixed layer. Similar patterns have also been shown for the other scyllarid and palinurid larvae collected in the present study (Table 2). 4. Discussion In the daytime, phyllosoma larvae of P. longipes and S. cultrifer were collected mainly from the base of the mixed layer (80 m depth layer), whereas in the nighttime they were collected in the surface water shallower than the base of the above mixed layer, though they were found from the surface down to 400 m depth. Regardless of the difference of day and night, most of the larvae (ca. 88% of all larvae collected) were collected in the surface water shallower than the base of the mixed layer. As mentioned in the section on Materials and Methods, contamination may not be neglected in retrieving the IKMT from 400 m depth. However, even if it were true, the features of vertical distributions of phyllosoma larvae that were made clear in the present study, may not be altered. A similar pattern has been observed by Austin (1972) in the Vertical Distributions of Phyllosoma Larvae in the Western North Pacific 745
4 Table 2. Vertical distributions of phyllosoma larvae in the present study. Fig. 3. Vertical distributions of phyllosoma and leptocephalus larvae by day and night during September 22 24, n: the number of the collected larvae; : daytime; : nighttime. The data for leptocephali were adapted from Kajihara et al. (1988). Gulf of Mexico where larvae of Panulirus spp. were mainly collected in the surface water (10 20 m depths shallower than the depth of base of mixed layer) both of day and night. On the other hand, according to Yeung and McGowan (1991), who examined vertical distributions of Scyllarus and Panulirus phyllosoma larvae in Florida waters, and to Rimmer and Phillips (1979) and Phillips et al. (1981) who deal with those of P. cygnus and S. bicuspidatus larvae in western Australian waters, most of the larvae extended into the thermocline in their diel vertical migrations, probably due to weaker thermocline than that observed in the present study and in Austin (1972). In the present study, phyllosoma larvae were dominated by the two species P. longipes (stages VI VIII) and 746 H. Minami et al.
5 S. cultrifer (stages IV VI) (Table 1). Regardless of species and life stages, these larvae showed almost similar patterns of vertical distributions to each other (Fig. 3). However, according to Rimmer and Phillips (1979) and Phillips et al. (1981), vertical distributions of phyllosoma larvae of P. cygnus and S. bicuspidatus changed depending on their life stages, though vertical distributions of P. cygnus larvae were similar to those of S. bicuspidatus larvae. According to Kajihara et al. (1988) dealing with leptocephalus larvae which were collected using the same sampling stations and gear as in the present study, vertical distributions of the larvae, including 10 specimens of A. japonica, were similar to those of phyllosoma larvae as illustrated in Fig. 3: most of leptocephalus larvae in the day were collected at 80 m depth, below which a strong thermocline and/or halocline developed. The spawning ground of A. japonica is located in the North Equatorial Current, i.e. in Mariana waters east of Luzon Island of the Philippines or west of Mariana Islands (Tsukamoto, 1992). Kimura et al. (1994, 1999) advanced a hypothesis to explain a long-distance transport of A. japonica leptocephalus larvae from Mariana waters to Japanese waters, suggesting that after the larvae had been transported westward by the North Equatorial Current, they may transfer to the Kuroshio Current due to Ekman transport by the trade wind and then may reach their growth habitats in Japanese waters through rapid transport due to the Kuroshio Current. We deduce from this that vertical distributions of phyllosoma larvae of both species P. longipes (stages IV VIII) and S. cultrifer (stages IV VI) were similar to those of leptocephalus larvae, as mentioned above, and that it takes 20 or more days after eggs hatching to get stages VI VIII of P. longipes and stages IV VI of S. cultrifer (Robertson, 1968; Ito and Lucas, 1990; Matsuda and Yamakawa, 2000). It is assumed that phyllosoma larvae collected in the present study may have been released in and transported from the water around the Mariana Islands. Most phyllosoma larvae collected in the present study belonged to the genera Scyllarus and Panulirus (Table 1). In general, Scyllarus phyllosoma larvae are found abundantly in coastal waters while those of Panulirus are found in offshore waters in meager numbers (Rimmer and Phillips, 1979; Phillips et al., 1981; Sekiguchi, 1986a; Inoue et al., 2000). Sekiguchi (1986a) and Inoue et al. (2000) suggest that Scyllarus phyllosoma may be retained within Japanese coastal waters north of the Kuroshio Current while those of Panulirus may be flushed out from the coastal waters and be retained within the Kuroshio Subgyre (the Kuroshio-Counter Current system). Similar phenomena have been reported from western Australian waters by Phillips and his colleagues (Rimmer and Phillips, 1979; Phillips et al., 1981) and from Japanese and Taiwanese waters by Sekiguchi (1986a) and Inoue et al. (2001). Inoue et al. (2001) proposed two alternative explanations for the abovementioned differences between horizontal distributions of Scyllarus and Panulirus phyllosoma larvae: (1) Panulirus have a much longer larval period than Scyllarus (Phillips et al., 1981), with the result that Panulirus may be transported to further offshore waters. Alternatively, (2) Panulirus are found in deeper layers than Scyllarus, with the result that Scyllarus may be retained within coastal waters while Panulirus may be transported to offshore waters. However, the latter explanation may be rejected, according to the present study (see Fig. 3) and also to Rimmer and Phillips (1979) and Phillips et al. (1981) because vertical distributions of Scyllarus were very similar to those of Panulirus. Acknowledgements The authors would like to express their heartfelt thanks to the captain and crew of R/V Hakuho-Maru all scientists for sampling on board. References Austin, H. M. (1972): Notes on the distribution of phyllosoma of the spiny lobster, Panulirus spp. in the Gulf of Mexico. Proc. Natl. Shellfish Assoc., 62, Booth, J. and B. F. Phillips (1994): Early life history of spiny lobster. Crustaceana, 66, Braine, S. J., D. W. Rimmer and B. F. Phillips (1979): An illustrated key and notes on the phyllosoma stages of western rock lobster Panulirus cygnus George. CSIRO Aust. Div. Fish. Oceanogr. Rep. 102, 13 pp. Cobb, J. S. (1997): Oceanic process affecting lobster larvae: report from a workshop. Mar. Freshwat. Res., 48, Cobb, J. S. and B. F. Phillips (1980): The Biology and Management of Lobster, Vol. 1. Academic Press, New York, 461 pp. George, R. W. and A. R. Main (1967): The evolution of spiny lobsters (Palinuridae): a study of evolution in the marine environment. Evolution, 21, Inoue, N. and H. Sekiguchi (2001): Distribution of late-stage phyllosoma larvae of Panulirus japonicus in the Kuroshio Subgyre. Mar. Freshwat. Res. (in press). Inoue, N., H. Sekiguchi and T. Nagasawa (2000): Distribution and identification of phyllosoma larvae in the Tsushima Current region. Bull. Japan. Soc. Fish. Oceanogr., 64, (in Japanese). Inoue, N., H. Sekiguchi and S. P. Yeh (2001): Spatial distributions of phyllosoma larvae (Crustacea: Decapoda: palinuridae and scyllaridae) in Taiwanese waters. J. Oceanogr., 57, Ito, M. and J. S. Lucas (1990): The complete larval development of the scyllarid lobster, Scyllarus demani Holthuis, 1946 (Decapoda, scyllaridae), in the laboratory. Crustaceana, 58, Kajihara, T., K. Tshukamoto, T. Otake, N. Mochioka, H. Hasumoto and M. Oya (1988): Sampling leptocephalus lar- Vertical Distributions of Phyllosoma Larvae in the Western North Pacific 747
6 vae with reference to the diel vertical migration and the gears. Nippon Suisan Gakkaishi, 54, Kanamori, K. (1982): Population ecology of Panulirus japonicus in Susami District, Wakayama Prefecture 1. Ann. Rep. Wakayama Pref. Fish. Exp. Sta., 1982, (in Japanese). Kanamori, K. and S. Kanamaru (1980): Population ecology of Panulirus japonicus in rocky shore waters along the Kumano-nada sea. Ann. Rep. Wakayama Pref. Fish. Exp. Sta., 1980, (in Japanese). Kimura, S., K. Tsukamoto and T. Sugimoto (1994): A model for the larval migration of the Japanese eel: roles of the trade winds and salinity front. Mar. Biol., 199, Kimura, S., K. Doos and A. C. Coward (1999): Numerical simulation to resolve the issue of downstream migration of Japanese eel. Mar. Ecol. Prog. Ser., 186, Matsuda, H. and T. Yamakawa (2000): The complete development and morphological changes of larval Panulirus longipes (Decapoda, Palinuridae) under laboratory conditions. Fisheries Sci., 66, Pearce, A. F. and B. F. Phillips (1993): In marine larval dispersal and recruit process: An interdisciplinary approach. p In Oceanic Processes, Puerulus Settlement and Recruitment of the Western Rock Lobster Panulirus cygnus, ed. by P. W. Sammarco and M. Heron, American Geophysical Union, Washington, D.C. Phillips, B. F. and M. C. McWilliam (1986): Phyllosoma and nisto stage of Scyllarus martensii Pfeffer (Decapoda, Scyllaridae) from the Gulf of Carpentaria, Australia. Crustaceana, 51, Phillips, B. F., P. A. Brown, D. W. Rimmer and S. J. Brain (1981): Description, distribution and abundance of late larval stages of the Scyllaridae (slipper lobster) in the southeastern Indian Ocean. Aust. J. Mar. Freshwat. Res., 32, Rimmer, D. W. and B. F. Phillips (1979): Diurnal migration and vertical distribution of phyllosoma larvae of western rock lobster Panulirus cygnus. Mar. Biol., 54, Robertson, P. B. (1968): The complete larval development of the sand lobster, Scyllarus americanus (Smith), (Decapoda, Scyllaridae) in the laboratory, with note on larvae from the plankton. Bull. Mar. Sci., 18, Roughgarden, J., S. Gaines and H. Possingham (1988): Recruitment dynamics in complex life cycle. Science, 241, Sekiguchi, H. (1986a): Spatial distribution and abundance of phyllosoma larvae in the Kumano- and Enshu-nada seas north of the Kuroshio Current. Bull. Japan. Soc. Fish. Oceanogr., 50, Sekiguchi, H. (1986b): Identification of late-stage phyllosoma larvae of the scyllarid and palinurid lobster in the Japanese waters. Bull. Japan. Soc. Sci. Fish., 52, Sekiguchi, H. (1997): Larval recruitment processes of Japanese spiny lobsters: a hypothesis. Bull. Mar. Sci., 61, Tanaka, T., O. Ishida and S. Kaneko (1984): Pueruli of three Panulirus species caught in rocky shore water of Chikura District, Chiba Prefecture. Suisan Zoshyoku (Aquaculture), 32, (in Japanese). Tsukamoto, K. (1992): Discovery of the spawning area for Japanese eel. Nature, 356, Yeung, C. and M. F. McGowan (1991): Difference in inshoreoffshore and vertical distribuion of phyllosoma larvae of Panulirus, Scyllarus and Scyllarus in the Florida Keys in May June, Bull. Mar. Sci., 49, Yoshimura, T., H. Yamakawa and E. Kozasa (1999): Distribution of final stage phyllosoma larvae and free-swimming pueruli Panulirus japonicus around the Kuroshio Current off southern Kyushu, Japan. Mar. Biol., 133, H. Minami et al.
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