A new species of echinoderid kinorhynch, Echinoderes sensibilis, is described and illustrated using light and electron microscopy. The specimens were collected from masses of the red algae Corallina pilulifera growing in intertidal pools in Tanabe Bay, Honshu Island, Japan. Diagnostic characters of E. sensibilis include the presence of middorsal spines on segments 6–10; lateral spines/tubules on segments 4, 7–12; remarkable trapezium-like subventral fields of minute cuticular hairs on segments 5-12. The positions of numerous sensory spots, large sieve areas, glandular tubes and the shape of terminal tergal and sternal extensions are also diagnostic. All taxonomic characters used for this description are illustrated by SEM. Echinoderes sensibilis constitutes the fifty-eighths valid species of the genus Echinoderes and the fourteenth species described from the Pacific Ocean. This is the third representative of Pacific kinorhynchs found only in the intertidal zone and the first Pacific Echinoderes living on red macroalgae in inter-tidal pools.
The Kinorhyncha constitute a taxon of meiobenthic, free-living, segmented and spined marine invertebrates, generally less than 1 mm in length. Previously, the taxon has been considered as a class of the phylum Aschelminthes (see Hyman, 1951), but currently is considered an independent phylum with close relationships to aschelminth worms (see Higgins, 1971; Kristensen and Higgins, 1991). Recently, the Kinorhyncha has been included as a class of the phylum Cephalorhyncha (see Adrianov and Malakhov, 1994, 1999).
Since the first description (Dujardin, 1851), about two hundred species of kinorhynchs have been described; of these 145 are valid/recognizable, others remain nomina dubia, species indeterminata or have been synonymized. According to the last taxonomic review on the Kinorhyncha (see Adrianov and Malakhov, 1999) and the most recent description (Sørensen et al., 2000), the genus Echinoderes consists of 57 valid species. Thirteen valid species of Echinoderes have been reported from the Pacific Ocean (see Adrianov and Malakhov, 1999).
A few studies have reported the presence of kino rhynchs (otherwise unidentified) from Japanese waters, and most of them were dealing with the ecology of subtidal meio-fauna. The first report of Kinorhyncha from Japan was Echinoderes sp. (Kawamura, 1927) collected by Komai in 1925 at Misaki Marine Biological Station near Tokyo (see Kawamura, 1927, 1947; Tokioka, 1949). Years later, Abe (1930) described a new species, Echinoderes masudai Abe, 1930, found at Gogoshima Island near Hiroshima. The description of the species was however too poor to do comparisons practically, and E. masudai is not currently designated as a valid species and considered as a “species indeterminata” (Higgins, 1983; Adrianov and Malakhov, 1999). In 1949, Tokioka reported another species of Echinoderes, E. dujardinii Claparède, 1863, from Ago Bay, Honshu Is. (Tokioka, 1949). Some years later, this species was listed by Sudzuki (1976a, b) from meiobenthic samples around Kasado Island in the Seto Inland Sea of Japan. The finding of E. dujardinii in Japan is however highly questionable because the species has been known only from European waters, and the reports of Tokioka (1949) and Sudzuki (1976a, b) seem to be misidentifications (see Higgins, 1983; Adrianov and Malakhov, 1994). Because of these facts, still no valid species of the genus Echinoderes has been reported from Japan.
The second genus reported from Japan was Kinorhynchus, listed and illustrated by Sudzuki (1976a) from the Seto Inland Sea of Japan and later identified as Kinorhynchus yushini Adrianov, 1989 (see Adrianov and Malakhov, 1999). Recently, Higgins and Shirayama (1990) described a new genus and new species, Dracoderes abei Higgins and Shirayama, 1990 from the Seto Inland Sea of Japan. Quite recently, the representative of the fourth genus, Pycnophyes tubuliferus Adrianov, 1989 was reported from Tanabe Bay in the vicinity of the Seto Marine Biological Laboratory of Kyoto University (Murakami et al., 2001).
This is the description of the fourteenth species of Echinoderes in the Pacific ocean. This is also the first detailed morphological study of Echinoderes from Japan using Nomarsky light microscopy and scanning electron microscopy (SEM).
MATERIALS AND METHODS
About one hundred specimens of the genus Echinoderes were collected in the washing of calcareous red algae, Corallina pilulifera Postels and Ruprecht, collected in March 2001 from intertidal pool in Tanabe Bay, located at Kii peninsula of Honshu Island (33°42.2′ N and 135°22.9′ E), in the vicinity of Seto Marine Biological Laboratory of Kyoto University (Fig. 1). All specimens were fixed in 10% buffered formalin in seawater. Specimens were transferred into a 70% ethanol - 5% glycerol - 25% deionized water solution. Letting ethanol and water evaporate, the material was preserved in anhydrous glycerol. Twenty specimens then were mounted individually in Hoyer's-125 mounting medium between two cover slips, and positioned on Higgins-Shirayama plastic slide frames for further examination using differential interference contrast optics (Nomarsky optics). About 30 specimens were selected for scanning electron microscopy (SEM). These specimens were transferred by an Irwin Loop from 10% formalin to a vessel of distilled water and washed using a detergent to clean the body surface. The cleaned specimens were transferred to a minimal volume of distilled water and ethanol was added slowly until the concentration became close to 100 percent. Thereafter, the specimens were washed in absolute ethanol several times, and finally replaced by tertiary-butyl alcohol. The specimens were dried in a freeze dryer, mounted on stubs, coated with Platinum-Palladium, and observed using a SEM (Hitachi S-4300).
In the examination procedures, we followed the standard protocol described by Higgins (1983). Measurements are given in micrometers. Ratios are expressed in percent of the Trunk length (TL) measured on the midline, from the anterior margin of segment 3 (first trunk segment) to the posterior margin of segment 13, exclusive of spines. Maximum sternal width (MSW) is measured at the anteroventral margin of the widest pair of sternal plates as first encountered in measuring each segment from anterior to posterior. Standard width (SW), or sternal width of segment 12, is measured at the anteroventral margin of 12th sternal plates. Measurements are given for length of trunk segments (L), lateral terminal spines (LTS), lateral terminal accessory spines (LTAS), middorsal spines (DS) and lateral spines/tubules (LS). The locality data from material examined are referred to the collector's initials (AVA and CM). The specimens in the code CM have been deposed in the meiofaunal collection of the Seto Marine Biological Laboratory of Kyoto University, and those in AVA in the meiofaunal collection of the Institute of Marine Biology in Vladivostok, Russia.
In the examination of taxonomic characters such are the nature, location and distribution of cuticular structures we followed the reevaluated interpretation of dorsal, lateral and ventral surface of the trunk that was proposed by Pardos, Higgins and Benito (see Pardos et al., 1998, Fig. 2) to achieve a more accurate approach to the descriptions of Echinoderes species. Specific terminology used in this paper mainly based on that developed by Higgins (1983) and Pardos et al. (1998). All diagnostic cuticular structures used in this description are illustrated by SEM to avoid misinterpretations of the characters.
Positions of cuticular structures on the trunk segments are termed as follows: middorsal (MD) - located on the middorsal line of the segment; paradorsal (PD) - located adjacent to the middorsal line of the segment; subdorsal (SD) - located lateral to the paradorsal position, closer to the middorsal line than to the maximum width of the segment; dorsolateral (DL) - located on the dorsal surface, closer to the point of maximum width of the segment than to the middorsal line; midlateral (ML) - located at the maximum width of the segment; sublateral (SL) - located between lateral accessory position and midlateral position; lateroventral (LV) - located on the tergal plate adjacent to the tergal-sternal articulation (position of lateral spines/tubules); lateral accessory (LA) - located on the tergal plate dorsally adjacent to the lateroventral position (position of lateral accessory spines/tubules); ventrolateral (VL) - located on the sternal plate adjacent to the tergal-sternal articulation; subventral (SV) - located on the sternal plate, between midvental articulation of sternal plates and ventrolateral position.
class Kinorhyncha (Reinhard, 1881) Pearse, 1936
order Cyclorhagida (Zelinka, 1896) Higgins, 1964
suborder Cyclorhagae (Zelinka, 1896) Zelinka, 1928
family Echinoderidae Bütschli, 1876
genus Echinoderes Claparède, 1863
Echinoderes sensibilis n. sp.
Echinoderes; basal plates of trichoscalids centered above subventral and subdorsal placids with incised anterior margin; middorsal spines on segments 6–10, short, less than half length of corresponding segment; lateral spines/tubules on segments 4, 7–12, lateral tubules on segment 12 slightly shifted dorsally to midlateral position; lateral spines on segment 8 clearly shorter than other lateral spines; terminal tergal extensions (furcae) pointed, with minute mesial projection bearing sensory spot; sternal plates of segments 5–12 with subventral trapezium-like fields of minute cuticular hairs; lateral terminal spines 43–47% of trunk length.
Masses of red algae, Corallina pilulifera Postels and Ruprecht, intertidal pools, Tanabe Bay, Kii-Peninsula, Pacific coast of Honshu Island, Japan (33°42.2′ N and 135°22.9′ E) (Fig. 1).
Holotype, adult male (CM-A-JAP-E04) (Fig. 2, 4A); allotype, adult female (AVA-C-JAP-E07) (Fig. 3, 4 B); paratypes - four adult males (AVA-C-JAP-E03; AVAC-JAP-E08; CM-A-JAP-E01; CM-A-JAP-E05) and four adult females (AVA-C-JAP-E09; AVA-C-JAP-E02; AVA-C-JAPE05; CM-A-JAP-E08).
Head; with 91 scalids arranged in 7 circlets; scalid formula 10,10, 20, 10, 20, 6, 15(6+9); enlarged basal plates of two subventral trichoscalids centered above subventral placids with deeply incised anterior margin.
Neck; with 16 placids, midventral placid largest, 18 μm high, 11 μm wide at top, 13 μm wide at base; subventral placids 16 μm high, 7 μm wide at base; middorsal placid 16 μm high, 8 μm wide at base.
First trunk segment; 35 μm in length; at anterior margin 69 μm wide; with dorsal pectinate fringe, ventral pectinate fringe undeveloped; with middorsal sieve area; with pair of ventrolateral sieve areas; with five pairs of sensory spots, in subdorsal, dorsolateral, midlateral, sublateral and subventral positions.
Length 34 μm; with dorsal and ventral pectinate fringe, with minute subventral units and enlarged ventrolateral and lateral units; with pair of lateral spines/tubules, 21 μm long; with middorsal sensory spot; with 2 pairs of sensory spots in dorsolateral position and one pair in subventral position.
Length 34 μm; with two sternal plates; maximum sternal width 53 μm; with dorsal and ventral pectinate fringe; sternal plates with rounded subventral field of minute cuticular hairs; with middorsal sieve area; with pair of subventral glandular pores; with 4 pairs of sensory spots, in subdorsal, dorsolateral, midlateral and sublateral positions.
Length 37 μm; maximum sternal width 58 μm; well developed pectinate fringe with minute subventral elements; middorsal spine short, 11 μm long; sternal plates with trapezium-like subventral field of minute cuticular hairs; sternal plates with transverse pectinate ridge of minute cuticular elements anterior to subventral field; with two pairs of sensory spots, in subdorsal and subventral positions.
Length 40 μm; maximum sternal width 64 μm; middorsal spine 12 μm long; with pair of lateral spines/tubules, 23 μm long; similar to segment 6 except for presence of one pair of midlateral sensory spots.
Length 42 μm; maximum sternal width 69 μm; middorsal spine 13 μm long; lateral spines/tubules 18 μm long; similar to segment 7 except for presence one pair of paradorsal sensory spots at base of middorsal spine.
Length 45 μm; maximum sternal width 71 μm; middorsal spine 16 μm long; lateral spines/tubules 23 um long; similar to segment 8 except for presence of pair of subventral glandular pores.
Length 48 μm; maximum sternal width 72 μm; middorsal spine 19 μm long; lateral spines/tubules 23 μm long; similar to segment 9 except for arrangement of cuticular elements on sternal plates; with pair of ventrolateral sensory spots, with pair of subventral sieve areas slightly posterior to transverse pectinate ridge of cuticular elements.
Length 52 μm; maximum sternal width 71 μm; lateral spines/tubules 24 μm long; similar to segment 10 except for lack of middorsal spine and pair of paradorsal sensory spots.
Length 55 μm; sternal width 69 μm; lateral tubules 27 μm long, shifted dorsally, between midlateral and dorsolateral position; ventral pectinate fringe with uniform cuticular elements; tergal and sternal plates with transverse pectinate ridge of minute cuticular elements at anterior margin; with two middorsal sieve areas, with pair of subventral sieve areas; with two pairs of sensory spots in subdorsal and ventrolateral position.
Length 37 μm; maximum sternal width 63 μm; terminal tergal extensions long, extending well beyond sternal plates, pointed, slightly fringed, with mesial projections at base; terminal sternal extensions slightly pointed, with pectinate fringe; sternal plates with transverse pectinate ridge of minute cuticular hairs, with pair of subventral cuticular scars slightly anterior to pectinate ridge; tergal plate with large sieve area in middorsal position; with three pairs of sensory spots, in subdorsal position, on mesial projections of terminal tergal extensions and at points of terminal sternal extensions; lateral terminal spines 155 μm long, 46% of trunk length; with three pairs of penile spines dorsally to gonopore at arthrocorium between segments 12 and 13, PS-1 35 μm, PS-2 24 μm, PS-3 32 μm.
Adult female (AVA-C-JAP-E07) (Fig. 3, 4B); TL 346 μm; L-3 34 μm, L-4 32 μm, L-5 34 μm, L-6 37 μm, L-7 40 μm, L-8 43 μm, L-9 45 um, L-10 48 μm, L-11 52 μm, L-12 55 μm, L-13 39 μm; anterior margin of first trunk segment 64 μm; MSW-5 52 μm, MSW-6 58 μm, MSW-7 64 um (19% of TL), MSW-8 71 μm, MSW-9 71 μm, MSW-10 71 μm, MSW-11 71 μm, SW 71 μm (21% of TL), MSW-13 58 um; DS-6 11 μm, DS-7 13 μm, DS-8 15 μm, DS-9 18 μm, DS-10 19 μm; LS-4 26 μm, LS-7 23 μm, LS-8 18 μm, LS-9 19 μm, LS-10 19 μm, LS-11 23 μm, LS-12 26 μm; LTS 148 μm, 43% of TL; LTAS 31 μm, 21% LTS.
Males differ from females in having three pairs of long penile spines (PS) and by slightly different arrangement of sensory spots, sieve areas and glandular tubes (Figs. 2–3, 6E). Females are also distinguished from males by the shape of anterior ventral pachycycli of segment 13 (Fig. 4). In contrast to males, females have more glandular pores scattered on segments 4–11 (Fig. 3).
Thirteen valid species of Echinoderes have been described from the Pacific Ocean: E. tchefouensis Lou, 1934 from the Yellow Sea (north-east China); E. pennaki Higgins, 1960 and E. kozloffi Higgins, 1977 from San Juan Archipelago (north-west of USA); E. newcaledonicus Higgins, 1967 from south-west Pacific (New Caledonia); E. pacificus Schmidt, 1974 from Galapagos Islands (east Pacific); E. nybakkeni Higgins, 1986 from the coast of California; E. filispinosus Adrianov, 1989, E. multisetosus Adrianov, 1989, E. koreanus Adrianov, 1999 and E. ulsanensis Adrianov, 1999 from the Sea of Japan; E. malakhovi Adrianov, 1999 from New Zealand; E. teretis Brown in Adrianov et Malakhov, 1999 and E. cavernus Sørensen, Jørgensen and Boesgaard, 2000 from Australia.
Echinoderes masudai Abe, 1930 and E. dujardini Claparède, 1863 reported from the Pacific coast of the mainland of Japan (Abe, 1930; Tokioka, 1949; Sudzuki, 1976a, b) are currently designated as “species indeterminata” and “misidentification” (Higgins, 1983; Adrianov and Malakhov, 1999). Echinoderes dujardini Claparède, 1863, very common in European waters, was carefully re-described by Higgins (1977). Like the new species, E. dujardini possesses very short middorsal spines on segments 6–10. However, this species is easily distinguished from E. sensibilis by the presence of lateral accessory spines on segment 10 and terminal setae on pointed sternal extensions of segment 13 (see Higgins, 1977).
Echinoderes sensibilis n. sp. resembles to E. multisetosus Adrianov, 1989 in having remarkable trapezium-like subventral fields of cuticular hairs on segments 5–12. However, E. multisetosus differs from the new species by the absence of middorsal spines. In addition, E. multisetosus is characterized by the presence of large oval paradorsal fields of cuticular hairs on segments 6–11, accessory lateral spines on segments 9–10 and a pair of subventral tubules on segment 11 (see Adrianov and Malakhov, 1999). Echinoderes filispinosus also is easily distinguished from the new species by the absence of middorsal spines like E. multisetosus, as well as the presence of remarkably elongated and sharp terminal tergal extensions and lateral spines/tubules only on segments 7 and 10. The only other Pacific Echinoderes without middorsal spines is E. malakhovi Adrianov, 1999 from New Zealand (see Adrianov and Malakhov, 1999). This species differs from E. sensibilis n. sp. by the presence of large subventral spines/tubules on segment 11. The most easily observed feature distinguishing E. teretis from Australia from E. sensibilis n. sp. is the presence of a single middorsal spine/tubule on segment 6 (see Adrianov and Malakhov, 1999). Echinoderes newcaledonicus Higgins, 1967 is easily distinguished from the new species by the presence of remarkably long middorsal spines on segments 6, 8 and 10 (see Higgins, 1967).
Measurement (mm) and indices (%) forEchinoderes sensibilisadults
Like the new species, eight other Pacific species of Echinoderes have middorsal spines on segments 6–10. Echinoderes koreanus Adrianov, 1999 from the south of the Sea of Japan well differs from E. sensibilis n. sp. by the size of middorsal spines which are clearly longer than the corresponding segments (see Adrianov and Malakhov, 1999). In contrast to the new species, the second Korean species, E. ulsanensis Adrianov, 1999 is characterized by remarkably short and thick lateral terminal spines (see Adrianov and Malakhov, 1999). Echinoderes tchefouensis Lou, 1934 from the Yellow Sea is distinguished from the new species by the presence of lateral spines/tubules only on segments 7, 10–11 (see Lou, 1934). Four species from the east Pacific, E. pennaki Higgins, 1960, E. kozloffi Higgins, 1977 from San Juan Archipelago, E. nybakkeni Higgins, 1986 from California and E. pacificus Schmidt, 1974 from Galapagos Islands, differ from E. sensibilis n. sp. by the size of the middorsal spines which are only slightly shorter or clearly longer than the corresponding segments (see Higgins, 1960, 1977, 1986; Schmidt, 1974). In contrast to the new species, all three species from the north-east Pacific have relatively long lateral terminal accessory spines. Echinoderes pacificus Schmidt, 1974 also differs from E. sensibilis n. sp. by the presence of long terminal setae on the pointed sternal extensions of segment 13 (see Higgins, 1977). Echinoderes cavernus Sørensen, Jørgensen and Boesgaard, 2000 from Australia is very similar to E. sensibilis n. sp. by the presence of very short middorsal spines on segments 6–10. However, E. cavernus is easily distinguished from the new species by the presence of remarkably short and thick lateral terminal spines and rounded tergal and sternal extensions of segment 13 (see Sørensen et al., 2000).
Echinoderes sensibilis n. sp. is the third Pacific species described only from the intertidal zone. Echinoderes kozloffi Higgins, 1977 was found in muddy sediments rich with detritus (see Higgins, 1977). Echinoderes nybakkeni Higgins, 1986 was described from the high-energy coarse beach sand (see Higgins, 1986). Echinoderes sensibilis n. sp. is the first Pacific species found in the washings of intertidal red algae.
Echinoderes sensibilis n. sp. constitutes the fourteenth valid species of Echinoderes in the Pacific and the first valid species of the genus described from Japan.
Abbreviations used in the figures
trapezium-like subventral fields of cuticular hairs
transverse cuticular ridge
lateral spine of segment 12
sieve area (pore sieve)
transverse pectinate ridge
penile spine followed by number of spine
prefix followed by segment number
slit-like glandular pore
tergal extensions of segment 13
basal plates of subventral trichoscalids
Acknowledgment is made to the Obuchi Foundation and their generous award of a fellowship to A. V. Adrianov that made possible to develop this cooperative research. Captain Y. Yamamoto and K. Okita (R/V Janthina II, Seto Marine Biological Laboratory, Kyoto University) helped sampling specimens. Part of this research also was supported by grant-in-aid of the Ministry of Education, Science, Culture and Sport, Japan (Dynamics of Ocean Biosystem, No. 12NP0201).