Deep-Sea Research II 86–87 (2013) 140–147
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Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2
Peanut worms of the phylum Sipuncula from the Sea of Japan
with a key to species
Anastassya S. Maiorova a,b,n, Andrey V. Adrianov a,b
a
b
A.V. Zhirmunsky Institute of Marine Biology, Far East Branch of Russian Academy of Sciences, Palchevskogo 17, 690059 Vladivostok, Russia
Far Eastern Federal University, Sukhanova 8, 690950 Vladivostok, Russia
a r t i c l e i n f o
a b s t r a c t
Available online 6 August 2012
Sipunculan worms from the Russian waters of the Sea of Japan are still poorly investigated while they
are much better known from the Japanese coast. The aim of this paper is to describe sipunculans from
the Russian coast and from the deepest part of the Sea of Japan near the Primorye Province collected by
SoJaBio expedition, and to provide keys for identification of sipunculan species from the Sea of Japan. At
the Russian coast of the Sea of Japan only 8 valid species of sipunculans were found and identified:
Golfingia margaritacea, G. vulgaris, Nephasoma capilleforme, N. wodjanizkii, Phascolion strombus, Thysanocardia nigra, Themiste hexadactyla ( ¼ T. pyroides), Phascolosoma agassizii. Taking into account 4 other
valid species noted for this area, Nephasoma eremite, Thysanocardia catharinae, Themiste blanda and
Phascolosoma scolops, which were not found, the sipunculan fauna of the Russian waters of the Sea of
Japan now comprises 12 valid species. Nephasoma capilleforme and Nephasoma wodjanizkii are the first
records for the North-West Pacific and the Sea of Japan. Species accounts include the most important
taxonomic characters and specific biotope data. Accordingly, a key up to species level is provided.
Totally, the fauna of the Sea of Japan is now estimated as having 31 valid species of sipunculans.
& 2012 Elsevier Ltd. All rights reserved.
Keywords:
The Sea of Japan
Peanut worm
Sipunculan
Introvert
Tentacular crown
Hooks
Trunk papillae
Contractile vessel
1. Introduction
Sipunculans, or peanut worms, constitute a well distinguished
monophyletic group of exclusively marine non-segmented coelom
worms which are currently considered as a separate phylum
Sipuncula. They are worldwide in distribution and live in a wide
variety of marine habitats from intertidal waters to abyssaldepths
and from polar to equatorial seas. After a series of taxonomic
revisions, about 150 valid species have been calculated currently
(see Cutler, 1994).
The body is subdivided into two main regions: barrel-like
trunk and long eversible introvert. The anteriormost introvert,
termed head, bears a terminal tentacular apparatus, the ciliary
tentacles of which function in gas exchange and in feeding.
The size of sipunculans varies considerably with trunk of
mature specimens (with retracted introvert) from 2–3 mm long
in meiobenthic Phascolion psammophilum (see Rice, 1993) and
3 mm in Onchnesoma steenstrupii to 500 mm in Siphonosoma
ingens, 550 in Sipunculus indicus (see Stephen and Edmonds,
1972), and even 600 mm in Sipunculus nudus (see Murina, 1977).
n
Corresponding author at: A.V. Zhirmunsky Institute of Marine Biology, Far East
Branch of Russian Academy of Sciences, Palchevskogo 17, 690059 Vladivostok,
Russia.
E-mail address: anastasia.mayorova@gmail.com (A.S. Maiorova).
0967-0645/$ - see front matter & 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.dsr2.2012.08.009
Most sipunculans are deposit feeders, although a few are filter
feeders, or sestonophages, with elaborate tentacular crown
(species of Thysanocardia and Themiste). Sipunculans consume
detritus and fecal material as well as bacteria, algae, protozoans
and small invertebrates. In turn, they are eaten by fish, gastropods
and cephalopods, carnivorous worms, crabs, starfishes, anemones,
and other predators, including men, and also used as a popular
‘fishbait’’.
Sipunculans may attain large densities as great as 700 specimens per m2 in reef limestone, and up to about 8000/m2 in some
soft sediments (Maiorova and Adrianov, 2010; Murina, 1984; Rice
et al., 1983; Williams and Margolis, 1974).
In soft sediments, some species live just a few centimeters
below the surface but some large species of Sipunculus burrow
down a meter in coarse or silty sands, making nearly vertical
tunnels. Many species live in sand-filled cracks, crevices, or
pockets in the rocks and may also be found in seagrass roots,
algal holdfasts and rhizoids, within sponges and under algal mats,
in byssal threads of mussels. Some species inhabit empty mollusk
shells, polychaete tubes, and foraminiferan tests. Several species
can bore into coral, rocks and in decaying whale skulls (Aspidosiphon, Cloeosiphon, Lithacrosiphon). Together with polychaetes,
sipunculans are designated to be the most important bioeroders
in many recent and fossil reefs. One species, Phascolosoma
turnerae, was found in association with submerged wood,
A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
occupying burrows in the wood (see Rice, 1985). Some small
sipunculans (e.g. Phascolion psammophilum) are interstitial in
coarse sand and shell hash.
One species, Phascolosoma saprophagicum, is found living only
on the flesh of a decomposing whale skull at about 900 m (see
Gibbs, 1987). Interestingly, that at the north coast of Sakhalin
Island in the Okhotsk Sea, sipunculan Golfingia margaritacea
(Sars, 1851) is an important component of the diet of grey whales,
in some areas comprising more than 50% of benthic biomass
(Maiorova and Adrianov, 2010).
About 30 species of sipunculans were found in the abyssal depth
(below 3000 m). Some eurybathic species are found between 10 and
4000 m over a wide range of temperatures but some species are
restricted to cold water deeper than 3000 m and never found above
this isobath. At least 13 species are known from the depth below
5000 m: Golfingia anderssoni (Theel, 1911); G. margaritacea (Sars,
1851); Golfingia muricaudata (Southern, 1913); Golfingia vulgaris
(de Blainville, 1827); Nephasoma capilleforme (Murina, 1973); Nephasoma diaphanes diaphanes (Gerould, 1913); Nephasoma flagriferum
(Selenka, 1885); Nephasoma minutum (Keferstein, 1862); N. schuettei
(Augener, 1903); Phascolion lutense (Selenka, 1885); Phascolion
pacificum (Murina, 1957); Onchnesoma magnibatha (Cutler, 1969);
Apionsoma murinae, (Cutler, 1969), (see Cutler, 1994). Some species
are common even at the ultra-abyssal depth (more than 6000 m)
(N. minutum, G. muricaudata, G. anderssoni, P. lutense, P. pacificum), but
it should be emphasized that the ultra-abyssal zone has no endemic
species.
Deeper cold-water species Sipunculus norvegicus Danielssen,
1869 is very common in seep communities near the mid-Atlantic
ridge at the depth from 1000 to 3500 m and provides a large
benthic biomass with high density in the local populations
(thousands of specimens per m2). When first collected in such
abundance in the deep-water seep communities during the MARECO (Mid-Ocean Ridges) expedition in July 2004, these large
worms, all being in the box-corers with retracted introvert, were
misinterpreted as priapulids and later identified to a species level
(see Maiorova and Adrianov (2010)).
Sipunculan fauna of the Far Eastern Seas (North-West Pacific)
is still not sufficiently investigated. Data of sipunculan fauna from
the Russian waters of the Bering and Okhotsk Seas and the Sea of
Japan can be found in a number of reports (see Adrianov and
Maiorova, 2010; Makarov, 1950; Maiorova and Adrianov, 2010;
Morozov and Adrianov, 2002; Murina, 1975, 1977; Ostroumov,
1909; Popkov, 1993a, 1993b).
In the Bering Sea, Makarov (1950) and Murina (1977) have noted
13 species of sipunculans. According to the modern synonymy (see
Cutler, 1994), 10 of them are now considered as valid species. These
species are G. muricaudata (¼G. appendiculata, in Murina, 1977),
G. margaritacea (¼ Phascolosoma margaritaceum, Phascolosoma hudsonianum, Phascolosoma glossipapillosum, in Makarov, 1950), G. vulgaris,
Nephasoma minutum, Nephasoma eremita (¼Phascolosoma eremite, in
Makarov, 1950 and Golfingia eremite, in Murina, 1977), N. diaphanes
(¼ Golfingia schuettei, in Murina, 1977), A. murinae (¼Golfingia
murinae, in Murina, 1977), Phascolosoma agassizii (¼P. japonicum, in
Makarov, 1950 and in Murina, 1977), Phascolion strombus
(¼ Phascolion strombi, in Murina, 1977).
In the Okhotsk Sea, about 15 species of sipunculans have been
listed (see Makarov, 1950; Murina, 1977), but only 11 of them are
now considered to be valid (see Cutler, 1994). These species
are G. vulgaris, G. margaritacea ( ¼Phascolosoma margaritaceum,
P. hudsonianum, P. wagini, in Makarov, 1950), N. eremita (¼P. eremite,
in Makarov, 1950 and G. eremite, in Murina, 1977), N. minutum
(¼Golfingia improvisa, in Murina, 1977), N. diaphanes (¼Golfingia
schuettei, in Murina, 1977), Thysanocardia catharinae (¼Golfingia
catharinae, in Murina, 1977), T. nigra (¼Phascolosoma pavlenkoi, in
Makarov, 1950), Themiste blanda, P. agassizii (¼P. japonicum, in
141
Makarov, 1950 and in Murina, 1977;¼P. kurilense, in Murina,
1977), P. scolops, Phascolion strombus (¼P. strombi, in Makarov,
1950 and in Murina, 1977).
In the Okhotsk Sea, we found four abundant species of peanut
worms—Golfingia vulgaris, G. margaritacea, P. strombus and Phascolosoma agassizii (Maiorova and Adrianov, 2010). P. agassizii is
the most common species in the Aniva Bay at the south-east coast
of Sakhalin Island, the north frontier of the natural habit (areal) of
this species.
In the Sea of Japan, Makarov (1950) and Murina (1975, 1977) have
listed respectively 10 and 21 species of sipunculans, most of them
being noted for Japan and Tsushima strait. Only 17 of them are now
considered to be valid (see Cutler, 1994). About eight of these species
have been noted for Russian waters from Tatarsky strait to the Peter
the Great Bay (Makarov, 1950; Murina, 1977). These species are:
Golfingia margaritacea (¼Phascolosoma margaritaceum, P. glossipapillosum, P. hudsonianum, P. okinoseanum, in Makarov, 1950; ¼Golfingia
ikedai, Golfingia glossipapillosa, G. nota, in Murina, 1977), G. vulgaris,
Thysanocardia catharinae (¼G. catharinae, in Murina, 1977), T. nigra
(¼Phascolosoma pavlenkoi, in Makarov, 1950; ¼Golfingia nigra, in
Murina, 1977), Themiste blanda, Phascolosoma agassizii (¼ P. japonicum, in Makarov, 1950 and in Murina, 1977; ¼ P. golikovi, in Murina,
1975; ¼P. yesoense, in Murina, 1977), P. scolops, Phascolion strombus
(¼P. strombi, in Makarov, 1950 and in Murina, 1977).
Two new species, Thysanocardia melanium and Themiste maculosa, described from the Peter the Great Bay by Popkov (1993a,
1993b), later were recognized as junior synonyms of Thysanocardia nigra (see Cutler and Dean, 1997) and of Themiste pyroides (see
Morozov and Adrianov, 2002).
A number of reports are available on the sipunculan fauna
from the Japanese and Korean waters (see Ikeda, 1904, 1924; Sato,
1930, 1934a,1934b, 1937; Cutler and Cutler, 1981; Cutler et al.,
1984; Cutler, 1994; Cutler and Dean, 1997; List of Animals in
Korea, 1998; Nishikawa and Ueshima, 2006).
About 30 species of peanut worms have been noted for the
eastern Sea of Japan, near the Japan Island and Tsushima strait
(see Cutler et al., 1984). Taking into account taxonomic revisions
(see Cutler, 1994), only 23 out of the listed species are considered
to be valid. For comparison, at the Pacific (east) coast of Japan
about 49 species have been listed (see Cutler et al., 1984).
In the List of Animals in Korea (1998), nine species of peanut
worms have been noted for Korean waters (Sipunculus nudus, T.
nigra, Themiste hexadactyla, Antillesoma antillarum, Phascolosoma
agassizii, P. albolineatum, P. japonicum, P. kurilense, P. scolops).
According to Cutler (1994), Themiste hexadactyla is a junior
synonym of T. pyroides and Phascolosoma japonicum and P.
kurilense are considered as junior synonyms of P. agassizii, thus
totally giving only seven valid species for this area.
The aim of this paper is to describe sipunculans from the Russian
coast and from the deepest part of the Sea of Japan near the
Primorye Province collected by SoJaBio expedition, and to provide
keys for identification of sipunculan species from the Sea of Japan.
2. Materials and methods
Sipunculans were collected and identified in the course of field
trips in the Russian water of the Sea of Japan during 2008–2010. Deep
water sipunculans were collected during the Russian–German deepsea expedition within the bounds of the SoJaBio-project (Sea of Japan
Biodiversity Studies) in August–September 2010. During the SoJaBio
voyage, benthic specimens were collected alongside the deep-water
transects from 500 to 3666 m near the Russian coast of the Sea of
Japan. Sipunculans from the Sea of Japan, available in the museum
collections, were also checked and identified.
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A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
Species accounts include quantitative characteristics and specific
biotope data. The material sampled was maintained in aquaria and
photographed alive for illustration of the tentacular apparatus and
live coloration of the body, introvert, and tentacles. Worms were fixed
with 10% formalin and then postfixed with 70% ethanol. Representatives of all species were examined for internal morphological observations and species identifications. Preparations of introvert hooks
were made for all species possessing these structures. Sipunculans
were examined using a light (Zeiss Axioplan) and scanning electron
microscope (LEO-430). The examined specimens are deposited in the
Museum of A.V. Zhirmunsky Institute of Marine Biology, Far Eastern
Branch, Russian Academy of Sciences (Vladivostok).
In taxonomic accounts we follow the synonymy suggested by
Cutler (1994).
3. Results
At the Russian coast of the Sea of Japan, we found and identified
only eight valid species of sipunculans: G. margaritacea, G. vulgaris,
N. capilleforme, N. wodjansky, P. strombus, T. nigra, T. hexadactyla
(¼T. pyroides), P. agassizii. Taking into account four other valid species
noted by Makarov (1950) and Murina (1977), N. eremite, T. catharinae,
T. blanda and P. scolops, which we were not able to find, the
sipunculan fauna of the Russian water of the Sea of Japan now
comprises 12 valid species. The fauna of the Sea of Japan is now
estimated as having 31 valid species of sipunculans.
Phascolosoma agassizii, P. scolops, T. nigra and T. hexadactyla
( ¼T. pyroides) usually inhabit the shallow water areas (0–50 m),
while G. margaritacea, G. vulgaris, N. capilleforme, N. wodjanizkii,
P. strombus are more deep water species, most common at the
depth from 50 to 1000 m. The deepest point where we found
G. margaritacea is the Bogorov elevation composed of lava stones
covered with mud at the depth 1699 m (SoJaBio).
Phylum Sipuncula Linnaeus, 1766
Class Sipunculidea E. Cutler and Gibbs, 1985
Order Golfingiiformes E. Cutler and Gibbs, 1985
Family Golfingiidae Stephen and Edmonds, 1972
Genus Golfingia Lankester, 1885
Subgenus Golfingia (Golfingia) Lankester, 1885
Golfingia margaritacea (Sars, 1851) (Fig. 1 A–D)
Material. Sea of Japan, near coast of Primorye Province,
SoJaBio-2010: sta# A2-8, trawl 44156.0262 N; 137113.2535 E,
582–570 m depth, gravel and muddy sediment, five specimens;
sta# B2-5, trawl, 42133.5243b N; 136117.5619 E, 1699 m depth,
lava stones with mud, five specimens; sta# B6-9, trawl, 43109.4745
N; 135100.5842 E; 1075 m depth, muddy sediment, eight
specimens.
Description. Trunk slender, cylindrical, 23–90 mm long and
6–10 mm wide; introvert about equal to the trunk length. Only one
young specimen has small scattered hooks, while all other mature
specimens lack this character. Trunk is pale and lustrous. Ventral
retractor muscles originate about 30% of trunk length to the posterior end. Dorsal retractor muscles originate in the anterior trunk, only
5–6% of trunk length to the posterior end. Gut with up to 35 loops.
Nephridia are about 10–15% of trunk length.
Discussion. Cutler (1994) has distinguished two subspecies—
G. margaritacea margaritacea (Sars, 1851) and G. margaritacea
ohlini (Theel, 1911). The last one is known only from the southern
hemisphere and differs from the nominate form by having hooks
(see Cutler, 1994). The only other species of the genus from the
Sea of Japan, G. vulgaris, is well distinguished from G. margaritacea
by rugose skin of the trunk and by the presence of well developed
hooks in mature specimens.
Distribution. This is the most widespread sipunculan species
in the North-West Pacific. In the Sea of Japan, this species
was previously known from Tatarsky strait and Sakhalin
Island in the north to Tsushima strait in the south, alongside
Korean, Japanese and Russian coast as well as in the middle
of the Sea.
Golfingia vulgaris (de Blainville, 1827)
Fig. 1. A–D, Golfingia margaritacea. (A) Lateral view, introvert retracted; (B) young specimen, lateral view, introvert everted; (C) head with tentacular apparatus;
(D) benthic sample from one Van Veen crab (0.025 m2) with amphipoda Ampelisca macrocephala. Scale bars: A, 20 mm; B, 10 mm; C, 2 mm; D, 50 mm.
A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
143
Genus Nephasoma Pergament, 1940
Subgenus Nephasoma (Nephasoma) Pergament, 1940
Nephasoma capilleforme (Murina, 1973)
Material. Sea of Japan, Peter the Great Bay, near cape Gamov
421200 5500 N; 1311230 4700 E, 200–300 m depth, grab, 6 specimens.
Description. Trunk spindle-shaped or thread-like, 3–12 mm
long, pale, with dark papillae concentrated at anus and posterior
end; introvert about equal to trunk length, with small scattered
hooks, tentacular crown with 6 tentacles. Retractor muscles
attached about 60% of trunk length to the posterior end. Gut with
12–15 loops. Nephridia about 15% of the trunk length, free.
Discussion. This species is well distinguished from two other
representatives of the genus Nephasoma from the Sea of Japan,
N. eremita and N. wodjanizkii, by the presence of hooks and by
elongate thread-like body. Trunk of N. capilleforme is usually
swollen and golden colored anteriorly, in the vicinity of anus
and nephridiopores, and possesses dark pigmented papillae at the
posterior end.
Distribution. The species was previously described only from
deep water areas of the Pacific, from Southern Hemisphere and
North-East Pacific, at the depth from 920 to 3450 m (see Murina,
1973, 1977). This is the first finding of N. capilleforme in the Sea of
Japan and the North-West Pacific.
Fig. 2. A–C, Themiste hexadactyla. (A) Lateral view, introvert everted (white
arrow – collar with patchy distributed pigment; white arrowhead-pigmented
anterior introvert); (B) head with tentacular apparatus; (C) hook. D–E, Themiste
blanda. (D) ventral view, introvert everted; (E) hook. F–G, Thysanocardia nigra.
(F) Lateral view, introvert everted; (G) head with tentacular apparatus. H–I,
Phascolosoma agassizii. (H) lateral view, introvert everted; (I) hook (black arrowhead – triangle of hook; black arrow-clear streak). Scale bars: A–B, 5 mm; C,
50 mm; D, 3 mm; E, 50 mm; F, 5 mm; G, 3 mm; H, 5 mm; I, 50 mm.
Material. Sea of Japan, Peter the Great Bay, near Nakhodka,
421310 06 N; 1321440 02 E, 200–300 m depth, grab, 10 specimens.
Description. Trunk elongated, spindle-shaped, 4–15 mm long and
2–3 mm wide; introvert shorter than trunk, with digitiform tentacles
and well developed scattered hooks in mature specimens. Trunk
yellow-brown with dark brown papillae more concentrated at the
anus and posterior end. Ventral retractor muscles originate about 30%
of trunk length to the posterior end. Dorsal retractor muscles
originate about 12% of trunk length to the posterior end. Gut with
about 16 loops. Nephridia are about 6% of trunk length.
Discussion. Cutler (1994) has distinguished two subspecies –
G. vulgaris vulgaris (de Blainville, 1827) and G. vulgaris herdmani
(Shipley, 1903). Animals belonging to the second subspecies differ
from the nominate form by having radiating rows of dark
spherical papillae at the posterior end, thus giving appearance
of the pseudoshield. This is shallow, warm water subspecies while
nominate form is mainly represented by deep and cold water
specimens. This species is well distinguished from G. margaritacea
by having well developed hooks in mature specimens. As noted
by Cutler (1994), G. vulgaris is characterized by dark brown or
black heavily papillated areas on the both ends of the trunk while
whitish middle trunk looks smooth. In our specimens from the
Sea of Japan, these dark brown papillae concentrating at the trunk
ends are also scattered over the whole body. Largest of these
specimens are also characterized by rugose skin with longitudinal
wrinkles in the middle trunk and radial wrinkles at the posterior
end, as noted for G. vulgaris herdmani.
Distribution. This species is widespread in the North-West
Pacific from shallow water to abyssal depth. In the Sea of Japan,
this species was previously known only from deep water near the
Russian and Korean coasts. This is the first record of this species
from the Peter the Great Bay.
Nephasoma wodjanizkii (Murina, 1973)
Material. Sea of Japan, near coast of Primorye Province,
SoJaBio-2010, sta# B7-8, trawl, 43113.6778 N; 135104.4447 E,
532 depth, muddy sediment, community of marine lilies Geliometra
glacialis, 4 specimens.
Description. Trunk 3.5 –23 mm in length; introvert 2–3 times
longer than trunk, with short tentacles, without hooks. Trunk pale,
brownish, with black pigmented anal area. Retractor muscles
attached about 75–85% of trunk length to the posterior end.
Gut with about 10 loops and 2 fixing muscles, oesophagus with
1 fixing muscle; spindle muscle present. Contractile vessel simple.
Nephridia 20–25% of the trunk length, dark brown, rough, free;
nephridiopores slightly anterior to the anus.
Discussion. The species was described by Murina (1973) from
the North-East Pacific based on a single specimen collected at
1100 m depth. In contrast to our material, small scattered hooks
were found on the introvert of this specimen. Another specimen
of N. wodjanizkii, but without hooks, was noted from the Canadian
coast by Frank (see Cutler and Cutler, 1986; Frank, 1983).
Thompson (1980) has described the new species, N. nicolasi, from
Californian, which was revised by Cutler as a junior synonym of
N. wodjanizkii (see Cutler and Cutler, 1986). No hooks have been
seen in Canadian and Californian specimens. As noted by Cutler
(see Cutler, 1994; Cutler and Cutler, 1986), in this genus some
species have hooks as young individuals but lose them with age
(deciduous hooks). In our specimens, nephridiopores open
slightly anterior to the anus while in all other specimens nephridia are situated slightly posterior to the anus. Despite this
difference, we identified specimens from the Sea of Japan as
representatives of N. wodjanizkii.
This species is well distinguished from other representatives of
the genus Nephasoma from the Sea of Japan, N. capilleforme and
N. eremita. In contrast to our species, N. capilleforme always has
hooks and is characterized by thread-like body and loosely wound
gut coil. Hookless N. eremita is characterized by nonpapillated
trunk with transverse grooves in the body wall and possesses well
developed digitiform tentacles. Also, in contrast to N. wodjanizkii,
retractor muscles of N. eremita originate in the middle of posterior
third of the trunk.
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A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
This is the first finding of N. wodjanizkii in the Sea of Japan and
the North-West Pacific.
Genus Thysanocardia (Fisher, 1950)
Thysanocardia nigra (Ikeda, 1904) (Fig. 2F and G)
Material. Sea of Japan, Peter the Great Bay, wide spread, muddy
sediments, rhizomes of seagrass Zostera marina, clusters of mussels Crenomytilus grayanus, Modiolus kurilensis and Mytilus trossulus, 1–10 m depth, more than 100 specimens.
Description. Trunk spindle-shaped, 20–60 mm long, 2–8 mm
wide; introvert one and one-half or two times longer than trunk,
with numerous tentacles arranged in dorsal and oral crowns, no
hooks. Tentacles in living specimens with wide yellow apical
bands followed by brown pigmentation. Trunk smooth, greyyellowish or gray, with minute papillae. Retractor muscles originate about 60% of trunk length to the posterior end. Gut with
18–54 loops, with two fixing muscles. Contractile vessel with
numerous pink or red digitiform or branched villi. Nephridia
about 30% of trunk length, free.
Discussion. This species was initially described from Japan (see
Ikeda, 1904) and redescribed in detail by Cutler et al. (1984).
Later, this species was noted from the north part of the Sea of
Japan (Sakhalin Island) (see Murina, 1977). The species, T. melanium,
described by Popkov (1993a) from the Possiet Bay (Peter the Great
Bay) in the west part of the Sea of Japan, was revised by Cutler and
Dean (1997) as a junior synonym of T. nigra because of only minor
differences with the nominate species from Japan.
Only other valid species of Thysanocardia, T. catharinae, has
been noted in the Sea of Japan. This species is known from
Russian (Primorye) and Korean (near Tsushima) waters (see
Murina, 1977). In contrast to T. nigra, tentacles of T. catharinae
are without brown pigmentation, only with yellow tips and
colorless in fixed specimens. This species is also distinguished
with characteristic sinuous (zigzag) wrinkles on the trunk which
tapers at the posterior end.
Distribution. T. nigra is tropical-boreal species, widespread in
the Pacific. In Russian waters T. nigra occurs from Tatarsky strait
in the north to Possyet Bay (Peter the Great Bay) in the south. In
the Sea of Japan, this species is also known from the Japanese and
Korean coasts. T. nigra was also noted from the Okhotsk Sea and
Pacific coast of Japan. In the West Pacific, the species is distributed to Indonesia. In the East Pacific, it is known from Washington to California. T. nigra is a shallow water species (0–200 m) and
was never found in the deep sea.
Family Phascolionidae E. Cutler and Gibbs, 1985
Genus Phascolion Theel, 1875
Subgenus Phascolion (Phascolion) Theel, 1875
Phascolion strombus (Montagu, 1804) (Fig. 3A–C)
Material. Sea of Japan: near coast of Primorye Province, SoJaBio2010, sta# A2-8, trawl 44156.0262 N; 137113.2535 E, 582–570 m
depth, gravel and muddy sediment, 8 specimens; sta# B7-8, trawl,
43113.6778 N; 135104.4447, 532 depth, gravel with muddy sediment, 7 specimens; 47140 N; 1391290 5 E in Tatarsky straight, 80 m
depth, 3 specimens; near Moneron Island 461N; 1411110 E, 320 m;
5 specimens.
Description. Trunk 15–20 mm long, 3–4 mm wide; introvert is
about twice longer than trunk, with claw-like scattered hooks.
Trunk with V-shape holdfast papillae on the posterior half. Gut
with loose loops, anus anterior to nephridiopores. Retractor
muscles originate about 80–90% of trunk length to the posterior
end. Nephridium about 25% of trunk length.
Discussion. The only other species of this genus in the Sea
of Japan is P. lucifugax representing the subgenus Phascolion
(Isomya). This species possesses dorsal and ventral retractor
muscles of equal size while in the subgenus Phascolion ventral
retractors are much thinner than dorsal ones. Cutler (1994) has
distinguished two subspecies of P. strombus – P. strombus strombus (Montagu, 1804) and P. strombus cronullae (Edmonds, 1980).
The last subspecies is known only from Australian waters and
differs from the nominate form by papillae morphology and by
proportion of retractor muscles.
Distribution. P. strombus is a very widespread species which
mainly inhabits various mollusk shells and polychaete tubes.
Young specimens can be found in the mouth of mollusk shells
occupied by adult worms (see Fig. 3B). In the Pacific, it is known
from both northern and southern hemispheres, at the depth from
1 to 4000 m. In the West Pacific, P. strombus is found from the
north part of Bering Sea to New Zealand. In the Sea of Japan, this
species was previously known from Russian (Primorye coast and
Tatarsky strait) and Japanese coasts (Honshu and Tsushima strait.
Family Themistidae E. Cutler and Gibbs, 1985
Genus Themiste Gray, 1828
Subgenus Themiste (Themiste) Edmonds, 1980
Themiste blanda (Selenka and de Man, 1883) (Fig. 2D and E)
Fig. 3. A–C, Phascolion strombus. (A) Lateral view, retracted introvert; (B) adult
specimen with retracted introvert in gastropod shell (white arrow, sipunculan
juvenile in the mouth of gastropod shell); (C) holdfast papilla. Scale bars: A–B,
3 mm; C, 50 mm.
Material. Sea of Japan, Tsushima strait, Cheju Island 331120 38 N;
1261150 41 E, intertidal, muddy clay, 12 specimens.
Description. Trunk pyriform, 3–6 mm long and 1.5–2.5 mm
wide; introvert about one-third of half of trunk length, with
scattered hooks covering anterior one-third of introvert; tentacular crown with four stems, with brown pigmented tentacules.
Gut with 3–4 loops, anus slightly anterior to nephridiopores.
Retractor muscles originate about 55% of trunk length to the
posterior end. Nephridia smooth, about 30% of trunk length, free.
Discussion. Two other valid representatives of the genus
Themiste, T. minor and T. pyroides, have been noted from the Sea
of Japan. T. hexadactyla is considered by Cutler (1994) as a junior
synonym of T. pyroides (see below). The taxonomic status of
A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
T. maculosa described by Popkov (1993b) is also controversial (see
below).
In contrast to T. blanda, another representative of the subgenus
Themiste (Themiste), T. pyroides, from the Sea of Japan possesses
large tentacular crown with six main stems, while representatives
from the North-East Pacific have only four main tentacles (see
Cutler and Cutler, 1988; Cutler, 1994). T. minor represents another
subgenus – Themiste (Lagenopsis) which is characterized by
contractile vessel with short digitiform villi while all representatives of the subgenus Themiste possess contractile vessel with
long thread-like processes.
Distribution. T. blanda is intertidal and shallow water species.
In the Sea of Japan, it was initially described from the Honshu and
Hokkaido Islands. Murina (1977) also noted this species from the
Okhotsk Sea and from the Russian coast of the Sea of Japan.
Themiste hexadactyla (Sato, 1930) (Fig. 2A–C)
Material. Sea of Japan, Peter the Great Bay, wide spread,
clusters of mussels Crenomytilus grayanus, Modiolus kurilensis
and Mytilus trossulus, 1–10 m depth, more than 150 specimens.
Description. Trunk spindle-shaped, cylindrical or pyriform,
10–60 mm long and 2–15 mm wide; introvert equal or slightly
longer than trunk, with black scattered hooks; tentacular crown
always with six branched stems in all ages, branches and stems
brownish at the aboral surface, separate tentacules with brown
bands in the middle. Tentacular crown followed by smooth area
(collar) with patchy distributed violet pigment (camouflage
drawing); in turn, this collar followed by smooth area with solid
violet or blue pigment. Trunk smooth, yellowish-brown or darkbrown, with minute papillae, usually with pointed posterior end.
Retractor muscles originate about 60–80% of trunk length to the
posterior end. Gut with 16–20 loops, with three fixing muscles;
anus and nephridiopores at the same level; wing muscles well
developed. Contractile vessel with numerous remarkably long
thread-like tubules. Nephridia about 80% of trunk length.
Discussion. The careful taxonomic revision appears to be
necessary for this genus in the near future to distinguish species
from the North-West and North-East Pacific.
Representatives of the genus Themiste are very numerous
in the Peter the Great Bay and, according to morphological
and genetic investigations, correspond to a single population of
one species (see Adrianov and Maiorova, 2010; Morozov and
Adrianov, 2002; Schulze et al., 2012). Taking into account Cutler’s
revision of the genus Themiste (see Cutler, 1994; Cutler and Cutler,
1988) and based on Cutler’s key to a species level (see Cutler,
1994), representatives of this species were identified as T. pyroides
(see Morozov and Adrianov, 2002). T. pyroides was initially
described from California (see Chamberlin, 1920) and later it
was noted from Alaska to Baja California in the North-East Pacific
and from Japan (Honshu and Hokkaido Islands) in the North-West
Pacific (see Cutler, 1994).
Themiste hexadactyla was initially described from Mitsu Bay of
Honshu Island in Japan (see Sato, 1930) and later this species was
also noted from Hokkaido (see Cutler and Cutler, 1981) and
California (see Cutler and Cutler, 1981; Fisher, 1952; Murina,
1977). The principal feature distinguishing T. hexadactyla from
T. blanda and T. pyroides is the presence of six main stems in the
tentacular crown (see Cutler et al., 1984, p. 282, Fig. 6D; Murina,
1977, p. 245, Fig. 169a; Sato, 1930). Nevertheless, Cutler and
Cutler (1988) introduce T. hexadactyla as a junior synonym to
T. pyroides and strike off this species from the key for the genus
Themiste (Cutler, 1994). In their new keys of the genus (see Cutler,
1994; Cutler and Cutler, 1988), he established for T. pyroides the
presence of six main stems of the tentacular crown.
145
To describe Themiste from the Possiet Bay (south part of the Peter
the Great Bay) with six tentacular stems, Popkov (1993b) has
suggested a new species, Themiste maculosa. He distinguished this
species from T. pyroides on the basis of the patchy (not solid)
distribution of pigment on the collar and rounded shape of the
posterior end of the trunk (see Cutler and Dean, 1997; Popkov, 1993).
Despite the hard criticism of Popkov’s description, Cutler and Dean
(1997) suggested confirming the validity of this new species thus
creating two nominate species with six tentacular stems.
Actually, according to our data, most specimens of T. pyroides from
American coast possess on the anterior introvert a wide solid purple
pigmented area without camouflage drawing, but all these specimens
are characterized by four tentacular stems (own observations).
In reality, all our specimens of Themiste from the Peter the Great
Bay, previously identified as Themiste maculosa with six tentacular
stems, possess patchy pigmented anteriormost introvert followed by
solid pigmented smooth area that is well seen in living specimens
with completely everted tentacular crown. Interestingly, that even in
living specimens with completely everted tentacles, this patchy
pigmented area can be partly or completely retracted into the
anterior introvert thus giving appearance of only solidly colored area
of the anteriormost introvert. Moreover, despite the presence of the
bluntly pointed posterior end in most living specimens, we have
observed some specimens of the same species with rounded posterior
end of the trunk.
Because of these facts, we do not recommend that only these
variable characters be used to introduce a new species of
Themiste. In this situation, we suggest to restoring validity of
T. hexadactyle for West Pacific Themiste with six tentacular stems
and considering T. maculosa as a junior synonym of this species.
Nominate T. pyroides and T. blanda are distinguished from
T. hexadactyla by the presence of only four main stems in the
tentacular crown. According to Cutler (1994, p. 151), T. pyroides
differs from T. blanda by much more voluminous tentacular crown
and shorter terminal tentacules. Other East-Pacific species of the
subgenus Themiste, T. dyscrita and T. hennahi, are well distinguished by the lack of hooks.
The last valid representative of the subgenus Themiste,
T. alutacea, is known only from Atlantic and characterized by
unpigmented collar of the introvert.
Distribution. T. hexadactyla is a shallow water East-Pacific
species depth range; in the Peter the Great Bay common in
between byssus threads and in slit-like spaces in clusters of
bivalve mollusks.
Class Phascolosomatidea
Order Phascolosomatiformes
Family Phascolosomatidae
Genus Phascolosoma Leuckart, 1828
Subgenus Phascolosoma (Phascolosoma) Leuckart, 1828
Phascolosoma agassizii Keferstein, 1866 (Fig. 2H and I)
Material. Sea of Japan, Peter the Great Bay, wide spread, clusters of
mussels Crenomytilus grayanus, Modiolus kurilensis and Mytilus trossulus, in clumps of sea grasses Zostera marina and Phillospadix iwatensis
on ground between stones, in muddy sand and mud substrates,
0–10 m depth, more than 200 specimens.
Description. Trunk cylindrical, 4–40 mm long and 1–10 wide;
introvert about equal to trunk length, with numerous hooks arranged
in distinct (15–30) rings. Trunk yellow-brown, brown or gray, with
large cupola-like dark brown or even black papillae over the whole
body, concentrating at anterior and posterior trunk. Tentacles with
dark blue or dark brown pigment at the bases. Hooks 45–65 mm tall
and 45–70 mm wide, with smooth streak and indistinct triangle,
without secondary tooth, with basal warts. Dorsal retractor muscles
originate about 50% and ventral retractor muscles about 60–65% of
146
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trunk length to the posterior end. Gut with 10–18 loops, with 1–3
fixing muscles, spindle muscle attached posteriorly. Anus at the same
level or slightly anterior to nephridiopores. Wing muscles well
developed. Nephridia about 30–50% of trunk length, about one-third
attached to the body wall.
Discussion. Four other species of the subgenus Phascolosoma
(Phascolosoma), P. scolops, P. pacificum, P. albolineatum and P. granulatum, have been known from the Sea of Japan. In contrast to P. agassizii,
P. scolops possesses introvert, usually shorter than trunk, hooks with
distinct triangle, and band of red cone-shaped preanal papillae. P.
pacificum is characterized by large (more than 100 mm tall) hooks with
hump-like secondary tooth and distinct triangle, and possesses very
long nephridia about equal to trunk length. P. albolineatum is well
distinguished by hooks bent at an obtuse angle. P. granulatum is a
species widespread in the Atlantic. P. granulatum, described from the
North-West Pacific, is now recognized as P. agassizii.
Cutler (1994) has distinguished two subspecies, P. agassizii agassizii
(Keferstein, 1866) and P. agassizii kurilense (Sato, 1937). The first
subspecies is known from North-East Pacific, from Alaska to Mexican
coast, and from Japan. The second subspecies is known only from
Kuril Islands and, in contrast to the nominate form, characterized by
the presence of secondary lobe in nephridia.
In Russian waters, P. agassizii has been noted from the Bering
Sea (¼P. japonicum; Komandor Islands), Okhotsk Sea (¼P. kurilense,
Kuril Islands; ¼P. japonicum, Sakhalin Island) and the Sea of Japan
(¼P. japonicum, Tatarsky strait, Peter the Great Bay, North Korea;
¼P. granulatum, Tsushima Strait).
Distribution. Common on both sides of the North Pacific from
Mexico to Alaska on the eastern side and from Japan to Russia in
the west. Scattered records from Indian Ocean waters, as well as
south and west Africa in the Atlantic.
4. Key to sipunculan species
In addition to our species, the following identification key also
includes all other valid species, lacking in Russian waters, but
noted from the Japanese and Korean coasts of the Sea of Japan
(see Murina, 1977; Cutler et al., 1984, 1994; List of Animals in
Korea, 1998; own collections).
1. Tentacular crown consists of oral crown with peripheral
tentacles arranged around mouth and on lateral sides of head;
tentacles of dorsal arc present or absent; hooks, if present, usually
scattered—class Sipunculidea (2)
Tentacular crown consists of dorsal arc encircling
nuchal organ; oral crown with peripheral tentacles absent;
hooks, if present, in distinct rings—class Phascolosomatidea (24)
2. Longitudinal muscles of body wall gathered into separate or
anastomosing bands—order Sipunculiformes, fam. Sipunculidae (3)
Longitidinal muscles of body wall in uniform continuous
layer—order Golfingiiformes (6)
3. Body wall circular and longitudinal bands anastomosing,
spindle muscle attached to the posterior trunk—genus
Siphonosoma (4)
Body wall circular and longitudinal bands not anastomosing,
spindle muscle not attached to the posterior trunk—genus
Sipunculus (5)
4. Dorsal retractor muscles originate anterior to ventral pair—S.
mourense
Retractor muscles originate at the same level—S. cumanense
5. 20–24 longitudinal muscle bands; nephridia free—S.
norvegicus
24–34 longitudinal muscle bands; nephridia 10–40% attached—S. nudus
6. Tentacular crown with four or six branched stems—fam.
Themistidae, genus Themiste (21)
Tentacles unbranched—(7)
7. Two nephridia present—fam. Golfingiidae (8)
One nephridium present—fam. Phascolionidae (18)
8. Contractile vessel simple, without villi—(9)
Contractile vessel with numerous digitiform villi genus
Thysanocardia—(17)
9. Four retractor muscles of introvert genus Golfingia—(10)
Two retractor muscles of introvert genus Nephasoma—(13)
10. Posterior trunk with prominent caudal appendage—
G. muricaudata
Posterior trunk without caudal appendage—(11)
11. Introvert hooks gathered in distinct rings—G. elongata
Introvert hooks scattered, if present—(12)
12. Introvert of mature specimens with hooks—G. vulgaris
Introvert of mature specimens without hooks—G. margaritacea
13. Tentacles reduced to lobes, trunk with pigmented papillae,
trunk length usually exceeds width by more than eight
times—N. diaphanes
Tentacles well developed, trunk with unpigmented papillae,
trunk length usually not exceeds width more than eight
times—(14)
14. Hooks present—(15)
Hooks absent—(16)
15. Body thread-like; hooks small (20–25 mm), scattered or
arranged in rings—N. capilleforme
Body not thread-like; hooks (50–150 mm) unique spirally
arranged—N. abyssorum
16. Trunk nonpapillated, with transverse grooves; retractor muscles originate in the middle third of the trunk—N. eremite
Trunk well papillated, without transverse grooves; retractor
muscles originate in the posterior quarter of the trunk—
N. wodjanizkii
17. Tentacular crown with dark pigment—T. nigra
Tentacular crown without pigment—T. catharinae
18. Retractor muscles fused into a single column; without
holdfast papillae—genus Phascolion, subgenus Phascolion
(Lesenka), P. rectum
Separate dorsal and ventral retractor muscles, with holdfast
papillae—(19)
19. Dorsal and ventral retractors of equal size—genus Phascolion, subgenus Phascolion (Isomya) (20)
Ventral retractor muscle much thinner than dorsal—genus
Phascolion, subgenus Phascolion (Phascolion), P. strombus
20. Hooks blunt, strongly curved; both retractor muscles
originate about 15% of distance from the posterior end
of trunk, ventral origin slightly posterior to dorsal one—
P. lucifugax
Hooks blunt, spine-like or slightly bent; two retractor muscles
originate at the same level at the posterior end of trunk—
P. hedraeum
21. Contractile vessel with long thread-like tubular extensions—
subgenus Themiste (Themiste) (22)
Contractile vessel with numerous digitiform villi—subgenus
Themiste (Lagenopsis), T. minor
22. Tentacular crown with six distinct stems, patchy pigmented collar followed by solid pigmented area—T. hexadactyla
Tentacular crown with four distinct stems, collar entirely
(solid) pigmented or non-pigmented—(23)
23. Anteriormost introvert with wide solid pigmented area,
purple or violet—T. pyroides
Anteriormost introvert non-pigmented or only slightly colored
apically with narrow band of brown-violet pigment—T. blanda
A.S. Maiorova, A.V. Adrianov / Deep-Sea Research II 86–87 (2013) 140–147
24. Anal shield always present, composed of numerous horny
plates, longitudinal muscles in continuous layer order Aspidosiphoniformes, fam. Aspidosiphonidae, genus Aspidosiphon,
subgenus Aspidosiphon (Aspidosiphon)—(25)
Anal shield always absent order Phascolosomatiformes, fam.
Phascolosomatidae—(26)
25. Anal shield with extensive grooves and furrows, individual
units form into longitudinal ridges—A. muelleri
Anal shield without extensive grooves and furrows—
A. misakiensis
26. Introvert several times (6 –1 4) longer than trunk; nephridia usually bilobed—genus Apionsoma (27)
Introvert usually not more than two times longer than trunk;
nephridia unilobed—genus Phascolosoma (28)
27. Tentacles present; hooks with accessory basal spinelets—
A. misakianum
Tentacles underdeveloped; hooks, if present, without spinelets—A. trichocephalus
28. Hooks remarkably bent at an obtuse angle—P. albolineatum
Hooks not bent at an obtuse angle—(29)
29. Hooks with hump-like secondary tooth and distinct triangle; nephridia about equal to trunk length—P. pacificum
Hooks without hump-like secondary tooth; nephridia much
shorter than trunk length—(30)
30. Introvert usually shorter than trunk; hooks with distinct
triangle—P. scolops
Introvert usually equal or longer than trunk; hooks with
indistinct triangle—P. agassizii
Acknowledgments
The authors gratefully acknowledge the support of the Russian
Foundation of Fundamental Research (grants 11-04-98546-r;
12-04-00263-a), the Far East Branch of the Russian Academy
of Sciences (grants 12-I-P30-07, 12-I-0-06-005, 12-I-0-06-004,
12-I-0-06-002, 12-HHC-007), APN Project ARCP2011-10CMY and
Ministry of Education and Science of Russian Federation (grant
11.G34.31.0010) during the course of this study.
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