Plankton Benthos Res 8(3): 107–115, 2013

Plankton & Benthos
Research© The Plankton Society of Japan

Aulographis japonica sp. nov. (Phaeodaria, Aulacanthida,
Aulacanthidae), an abundant zooplankton in the deep seaof the Sea of JapanYASUHIDE NAKAMURA1,*, ICHIRO IMAI1, ATSUSHI YAMAGUCHI1, AKIHIRO TUJI2 & NORITOSHI SUZUKI3
1

Plankton Laboratory, Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, 041–8611, Japan
Department of Botany, National Museum of Nature and Science, Tsukuba, 305–0005, Japan.
3
Institute of Geology and Paleontology, Graduate School of Science, Tohoku University, Sendai 980–8578, Japan
2

Received 7 March 2013; Accepted 10 May 2013
Abstract: Zooplankton samples from the deep water of the Sea of Japan often contain yellowish semitransparent
spheres (1.0–1.5 mm in diameter). We recognized these spheres as a single phaeodarian species (Cercozoa, Rhizaria)
and described them as Aulographis japonica sp. nov. (family Aulacanthidae) in this paper. This species has a highabundance in the Japan Sea Proper Water (JSPW) and occasionally higher biomass than that of copepods. Molecularanalysis based on 18S SSU rDNA revealed that Aulacantha scolymantha, which belongs to the same family as
A. japonica, is closer to Aulosphaera trigonopa and Protocystis spp., which belong to different orders, than to thepresent species. The distribution of A. japonica is apparently restricted to low temperature water. Its biomass was thehighest in the uppermost layer of JSPW, and this phaeodarian species was the second most important zooplankton
below 250 m depth in terms of biomass among the total zooplankton groups. This is probably due to its generalist
type of feeding. Considering its large biomass, A. japonica possibly plays an important role in matter cycles within
the Sea of Japan.
Key words: Aulographis japonica, Cercozoa, new species, Phaeodaria, the Sea of Japan

Introduction
The deep water in the Sea of Japan has a unique hydrography with its own particular fauna. The central area of the
Sea of Japan is deeper than 3,000 m, while the four straits
that connect it to the surrounding seas are relatively shallow. Through these four straits, surface water can be exchanged with the open sea (Nishimura 1974). By contrast,
the deeper water below 300 m depth is characterized by aconstant low temperature (ca. 1°C) and salinity (ca. 34),
and this stable water mass is called the Japan Sea Proper
Water (JSPW) (Uda 1934, Nishimura 1974). The isolatedhydrographic properties of JSPW are supposed to contribute to the low reported diversity of zooplankton in this sea
area (e.g. Nishimura 1974, Horikoshi 1996). In the JSPW,
we found an abundance of a protozoan zooplankton of 1.0–
1.5 mm in diameter, the form of which resembles a yellow* Corresponding author: Yasuhide Nakamura; E-mail, y.nakamura@ﬁsh.
hokudai.ac.jp

ish ﬁsh egg, and this zooplankton was identiﬁed as a
species of phaeodarian.
The subclass Phaeodaria is a holoplanktonic marine protistan group, belonging to the phylum Cercozoa of theinfrakingdom Rhizaria (Nakayama 2011) and was formerly
considered to be a group within the Radiolaria (Suzuki &Aita 2011). They are mainly distributed in the deep sea
worldwide and in cold surface waters in the Polar Regions(Reshetnyak 1955). The cell size of Phaeodaria ranges
from several tens of micrometers to a few millimeters, andPhaeodaria are recognizable by the presence of a delicate
opal skeleton that contains a double-layered spherical protoplasmatic body named the central capsule, and a mass ofbrown aggregated particles called the phaeodium. In our
sampling cruise in the eastern margin of the Sea of Japan,
west of the Japanese Islands, in June 2011, we found amarked abundance of phaeodarians in the deep sea. Ourcareful observations of the skeletal and protoplasmic characteristics of these phaeodarians proved that they belong toa single species. Further morphological examination and108

Y. Nakamura et al.

genetic analysis revealed that the species belongs to thegenus Aulographis but differs from hitherto-known species of the genus. We describe it as a new species, andbrieﬂy discuss its ecological roles in the Sea of Japan.
Materials and Methods
Sampling
Plankton samples were collected using a Vertical Multiple Plankton Sampler (VMPS; mouth opening 0.25 m2,
mesh size 60 µm) at two stations, Sta. SJ1 (41°59′N,
138°21′E) and Sta. SJ2 (38°28′N, 135°30′E), in the Sea ofJapan on 15 and 21 June 2011, during a cruise of the T/SOshoro-Maru (Hokkaido University) (Fig. 1). At each station, we sampled 12 layers: 0–25, 25–50, 50–75, 75–100,
100–150, 150–250, 250–500, 500–750, 750–1000, 1000–
1500, 1500–2000 and 2000–3000 m depth. After sampling,samples were immediately ﬁxed and preserved in 5%
borax-buffered formalin-seawater on board.
For molecular phylogenetic analysis, we also sampledwith a Gamaguchi-net (mouth opening 60 cm, mesh size
60 µm; Kawamura 1989) from the 250–750 m layer at Sta.
SJ3 (41°52′N, 139°06′E) and at Sta. SJ4 (41°37′N, 139°14′E)
on 24 and 25 April 2012, during a cruise of the T/S UshioMaru (Hokkaido University) (Fig. 1). After sampling, eachsample was immediately divided into two aliquots. One of

the aliquots was immediately preserved in 5% boraxbuffered formalin-seawater, while the other one was used
to isolate phaeodarian individuals for genetic analysis. A
hundred individuals were extracted from the sample undera stereomicroscope, and then each individual was put into
separate wells of a cell culture plate. After incubation at
4°C for 12 hours to cleanse them, they were separately
preserved in approximately 2.0 mL of 99.9% ethanol.
Water temperature and salinity were measured with a CTD
system (SBE911plus, Sea-Bird, U.S.A.).
Microscopic observation and estimation of biomass
For an examination of morphological characters, 120
individuals were extracted from the 24 formalin-preserved
samples from Sta. SJ1 and Sta. SJ2 under a stereomicroscope, and their morphological variations and differenceswere examined under an inverted microscope at 50 to
400X magnitudes. Examined phaeodarian individuals
were photographed with a digital camera (DIGITALSIGHT DS-Ri1, Nikon, Japan) attached to the microscope.
For detailed examinations of the ﬁne structures, 20 individuals that were selected under an inverted microscopewere observed with a SEM (JSM-6390 with LaB6 gun,
JEOL, Japan). They were mounted on specimen stubs
under a stereomicroscope and were gently dried at 60°C ina dry heat sterilizer overnight, prior to coating with platinum.
To estimate the biomass of phaeodarians, the formalinpreserved samples were analyzed using an Optical Plankton Counter (OPC-1L, Focal Technology Corp., Canada).
Almost all the zooplankton in these samples were ﬁrst
sorted out according to taxa, and subsamples of each taxon
were prepared. The number of zooplankton in each subsample was then counted to estimate the abundance ofeach taxon. These subsamples were analyzed through the
OPC, and the estimated spherical diameter (ESD) of eachtaxon was measured. From the mean ESD, the wet-mass
biomass (mg WM m−3) of each taxon was calculated on the
supposition that the speciﬁc gravity of zooplankton isequal to that of water.
Molecular analysis

Fig. 1. Location of sampling stations in the Sea of Japan inJune 2011 (Sta. SJ1 and Sta. SJ2) and in April 2012 (Sta. SJ3 andSta. SJ4).

Two ethanol-preserved specimens of this phaeodarianspecies, one from Sta. SJ3 and another one from Sta. SJ4,
were analyzed in this study. These specimens wereobserved under the inverted stereomicroscope to conﬁrm
that there was no contamination due to other organisms on
or in the specimens, and images were recorded as evidence
for the morphological identiﬁcation. After being dissectedwith a sterilized scalpel, their central capsules (protoplasmic body with nucleus) were transferred into 50 µL of
GITC buffer, preserved in −80°C overnight and thenheated at 70°C for 20 min to break the wall of the central
capsule. DNA was puriﬁed with a chemagic DNA Plant kit(Chemagen, Germany).
The PCR ampliﬁcation for the small subunit (SSU) ribo-

109

A new phaeodarian species from the Sea of Japan

Table 1. List of primers used for PCR and sequences in this study.
PrimerPhaeoF
Medlin B
Medlin A
PhaeoR

Sequence 5′-3′

Direction

Remarks

CCTCTTTAGGTCTGGTAATTGG
CCTTCTGCAGGTTCACCTAC
AACCTGGTTGATCCTGCCAGTGGCCAYTRAATACTAGCACC

forwardreverseforwardreversenewly designed for this study
Medlin et al., 1988
Medlin et al., 1988
newly designed for this study

somal DNA was carried out using a thermal cycler (GeneAmp PCR system 9700, ABI, U.S.A.). The reaction volume was 25 µL, and the solution consisted of 1.0 µL template DNA, 0.35 µM of each primer, 12.5 µL Ampdirect
Plus (Shimazu, Japan), 9.625 µL H2O and 0.125 µL KAPA
3G Plant DNA Polymerase (Nippon Genetics Co. Ltd,
Japan). Two primer sets were used (Table 1). PhaeoF andPhaeoR were phaeodarian-speciﬁc primers and designed
for this study. PCR reactions were performed using the following protocol: initial denaturation at 95°C for 5 min, 40
cycles at 95°C for 30 sec, 50°C for 30 sec and 72°C for
60 sec with a ﬁnal extension at 72°C for 7 min. The ampliﬁed PCR products were puriﬁed with ExoSAP-IT (USB
Corporation, U.S.A.). Sequencing reactions were conducted using an ABI PRISM 3130xl Genetic Analyzer(ABI, U.S.A.).
The obtained sequences were assembled using ChromasPro (Technelysium Pty Ltd, Australia), and the alignments were checked manually. The sequences were registered in the DNA Data Bank of Japan (SJ3: AB820365,
SJ4: AB820366). In order to examine the phylogenetic
relationship between the present species and other phaeodarians, the sequences of nine other species were obtained
from the Basic Local Alignment Search Tool (BLAST) at
NCBI (http://blast.ncbi.nlm.nih.gov/Blast.cgi). Phylogenetic analyses of the obtained sequences were conductedusing the computer program MEGA 5 (Tamura et al. 2011).
The General Time Reversible (GTR) model plus Gamma
with the shape parameter for among-site rate variation (G)was selected based on the lowest BIC (Bayesian Information Criterion) score, and the substitution nucleotide matrix
parameters were calculated. A maximum-likelihood (ML)tree was constructed with the selected model by the
program. Bootstrap values (Felsenstein 1985) for neighborjoining (NJ) and ML methods were estimated, and the two
calculations were performed for 1000 replicates and 100
replicates, respectively.
Results
Systematic descriptions
Aulographis japonica Nakamura, Tuji et Suzuki sp. nov.
Examined specimens: 60 individuals from Sta. SJ1 and 60
individuals from Sta. SJ2.

Dimensions: Malacoma is 1.11–1.59 mm in diameter(x̄=1.37, n=50). Central capsule is 0.22–0.27 mm in diameter (x̄=0.24, n=100). Terminal branch is 18.1–25.0 µm(x̄=21.7 µm, n=33) long.
Type material: All type material from sample OS11019 in
Plankton Laboratory, Hokkaido University.
Holotype: A mounted stub MPC-03709 (Fig. 4A–F).
Paratypes: A mounted slide MPC-03710 (Fig. 2A–C). An
ethanol-ﬁxed specimen MPC-03711 (Fig. 2 D–F).
The specimens with the acronym MPC are deposited in
the Micropaleontology Collection, Department of Geology
and Paleontology, National Museum of Nature and Science, Japan. Other paratypes and extracted DNA are kept
at the Center for Molecular Biodiversity Research, National Museum of Nature and Science, Japan.
Type locality: Sta. SJ1 (41°59′N, 138°21′E) in the Sea ofJapan.
Description: Malacoma spherical, large, consisting of twoor rarely three central capsules (Figs. 2A, 2D, 3A), phaeodium, and spherical calymma. Central capsule globular orsometimes distorted, and deep brown in color. Phaeodium
consisting of aggregated small brown granules, concentrated in center of malacoma, and generally bigger thancentral capsule. Scleracoma composed of spherical veiland several hundred radial spines. Spherical veil comprised of very thin, tube-like, and cylindrical shaped tangential needles forming a hollow sphere. Radial spines
long, cylindrical and distally tapered; 1/8 to 1/12 exposedout from spherical veil. Distal end of radial spine forming
distal crown, having three or four terminal branches eachwith four to six peripheral teeth and sometimes one apicaltooth on distal end. Peripheral tooth conical, directed
obliquely outward and surrounding end of spathilla (Figs.
2C, 2F, 3C, 4B–F).
Systematic remarks: This new species is characterized by
the radial spines possessing several obliquely outwarddirected peripheral teeth on the spathilla of the terminal
branch, and by the absence of a dentate terminal branch.
Peripheral teeth never bend back like a ﬁshhook. Amongthe 32 previously described Aulographis species, similarmorphological characters to the new species are recognized in the following six species: A. ﬂammabunda
Haeckel, 1887, A. hexancistra Haeckel, 1887, A. mohriTibbs, 1976, A. pentastyla Haecker, 1908, A. tetrancistra
Haeckel, 1887 and A. triama Haeckel, 1887. Aulographis
japonica sp. nov. is easily distinguished from A. ﬂamma-

110

Y. Nakamura et al.

Fig. 2. Paratype specimens (MPC-03710: A–C, MPC-03711: D–F) of Aulographis japonica sp. nov. A, D: Whole cell. B, E:
Radial spines with terminal branches. C, F: Terminal branches with peripheral teeth directed outward and upward.

bunda by having pronounced branched distal crowns andfrom A. triama which has irregularly-ramiﬁed spathilla.
This new species differs from A. hexancistra and A. mohriwhich have a dome-shaped tip on the spathilla, and fromboth A. pentastyla and A. tetrancistra, which have spiny
spathilla but no conical teeth. The morphological characters distinguishing it from the remaining three species arelisted in Table 2 and Fig. 5.
Etymology: Derived from the distribution area of this new
species.

Molecular phylogenetic analysis
The phylogenetic tree constructed with the two Aulographis japonica sp. nov. specimens and nine phaeodarianspecies registered in the NCBI database (Fig. 6) showedthat the species analyzed were dividable into twogroups, i.e. the species (Coelodendrum ramosissimum andConchellium capsula) belonging to the order Phaeoconchia
and the other eight species of the other orders. The lattergroup was subdividable into four clades, one of whichsolely contained A. japonica.

111

A new phaeodarian species from the Sea of Japan

Fig. 3. Schematic illustration of Aulographis japonica sp. nov. A: Malacoma. B: Radial spines with terminal branches. C:
Terminal branches with peripheral teeth directed obliquely outward. Note that most radial spines are omitted.
Table 2. Comparison between different species of the genus Aulographis.
A. hexancistra
Haeckel, 1887

A. tetrancistra
Haeckel, 1887

A. mohriTibbs, 1976

A. japonica
sp. nov.

1.60
3–8(generally 5–6)
4–6
(strongly recurved)
1–2
North Paciﬁc,Indian South Equatrial Cur.
Antarctic
1, 5, 11

1.20–1.50
3–6(generally 4)4(strongly recurved)
0
widespread(except the high Arctic)

1.20–1.40
2–4(generally 3)
4–8(strongly recurved)
0–1*
Antarctic

1.11–1.59
3–4
4–6(obliquely outward)
0–1
Sea of Japan

1–13

11, 13This study

SpeciesMalacoma size (mm)No. of terminal branches
No. of peripheral teeth
No. of apical teeth
Distribution
References*** Tibbs (1976) described as “apical process”.
** Haeckel 1887, Borgert 1901, Wolfenden 1902, Immermann 1904, Haecker 1908, Jorgensen 1907, Schroeder 1913, Peters 1928, Dogiel& Reshetnyak 1952, Reshetnyak 1966, Tibbs 1976, Takahashi 1991, Kling & Boltovskoy 1999.

Vertical distribution of biomass
The sea surface temperature at Sta. SJ1 was 13.4°C. The
temperature decreased with depth and became almost constant ca. 0.5°C below 400 m depth (Fig. 7A). The watertemperature at Sta. SJ2 was 20.2°C at the sea surface andthen decreased. The temperature below 400 m depth wasnearly constant, ca. 0.5°C. The salinity at Sta. SJ1 was 33.8
at the sea surface and increased to ca. 34.0 with limited
ﬂuctuation down to 250 m depth. The salinity becamealmost constant, ca. 34.0, below 250 m depth. The salinity
at Sta. SJ2 greatly varied from 33.9–34.5 above 250 m,
while below 250 m it was almost stable at ca. 34.0. Consid-

ering the temperature of ca. 0.5°C and salinity of ca. 34.0,
the water masses below 400 m at the two stations are classiﬁed as typical Japan Sea Proper Water (JSPW) (Sudo1986).
Aulographis japonica sp. nov. was found throughout thewater column below 250 m depth at Sta. SJ1 and SJ2,
whereas it was never found above 250 m depth. Zooplankton collected with the VMPS below 250 m at both stations
consisted mainly of copepods (e.g. Neocalanus spp.),
Aulographis japonica, euphausiids, ostracods and amphipods. The biomass of A. japonica below 250 m was higher
in shallower layers than in deeper layers at both stations(Fig. 7B, E). At Sta. SJ1, the biomass reached the maxi-

112

Y. Nakamura et al.

Fig. 4. Scanning electron micrographs of Aulographis japonica sp. nov. (Holotype specimen). A: Whole cell. B–F: Radial
spines with terminal branches possessing different numbers of teeth. Note that close-up photographs are also shown in every
panel.

mum of ca. 40.0 mg WM m−3 in the 500–750 m layer andbecame nearly constant (2.0–4.0 mg WM m−3) below
750 m (Fig. 7B). At Sta. SJ2, the maximum biomass of thespecies was 10.7 mg WM m−3, in the 500–750 m layer, andbecame lower ranging 0.7–3.1 mg WM m−3 in the deeper
layers (Fig. 7E). The proportion of A. japonica with respect

to the total zooplankton biomass below 250 m ranged from
7.8–24.5% at Sta. SJ1 (Fig. 7C). In contrast, the relative
proportion comprised by this species showed a different
pattern at Sta. SJ2, where it was relatively low in the layers
between 250 m and 2,000 m water depth, with a peak of
11.3% in 500–750 m layer. However, the relative propor-

A new phaeodarian species from the Sea of Japantion of biomass comprised by this species reached 71.9% in
the 2,000–3,000 m layer (Fig. 7F). The mean proportion
below 250 m depth at the two stations was 22.3%, which
was the second largest, following that of copepods (66.6%).
Discussion
The present result of the molecular phylogenetic analysis
is very mysterious because the relationships in the tree
differ greatly from the morphology-based, current systematics of the Phaeodaria. For example, Protocystis xiphodon
and P. tridens of the order Phaeogromia were closer to
Aulosphaera trigonopa of the order Phaeosphaeria than toFig. 5. Schematic illustrations of terminal branches of different
species belonging to the genus Aulographis.

113

Challengeron diodon and Medusetta arcifera, which
belong to the same order as Protocystis spp. In addition,
Aulacantha scolymantha of the same family Aulacanthidae
as the present species was closer to Aulosphaera trigonopa
and Protocystis spp., which belong to different orders, than
to the present species. Since such a discrepancy between
the present results and current systematics is very unlikely,
the mysterious result is possibly attributable to some
unknown problems with the genetic data used here.
Species belonging to the genus Aulographis are distributed worldwide in the deep sea, below 200 m (Reshetnyak1966). Reshetnyak (1966) examined the phaeodarian faunain the Sea of Okhotsk, the Bering Sea and the Kuril–
Kamchatka region, but she did not record any species
referable to A. japonica. We carefully examined plankton
samples collected from 0–3,000 m depth in the western
North Paciﬁc in 2007 and stocked in Hokkaido University,
but never found A. japonica in any of these samples (ourunpublished data). These facts suggest that the distributionof this species is restricted to the Sea of Japan. In addition,
the present result, that A. japonica was never collectedfrom the layers above 250 m depth but was abundant in
the 250–500 m and deeper sampling layers, suggests the
species is endemic to JSPW.
Meyer (1933) examined the vertical distribution of phaeodarians in the Atlantic and classiﬁed them according to
the water temperature at the sampling depths. He notedthat the distribution of phaeodarians is presumably dependent on the water temperature because the species found indeep waters at low latitudes were also collected from shallower waters in high-latitudes in the North Atlantic. Considering that Aulographis species were distributed in cold
waters in the Atlantic (Meyer 1933), the distribution ofFig. 6. Phylogenetic tree of Aulographis japonica sp. nov. and other phaeodarian species based on SSU 18S rDNA alignments
and the Maximum-likelihood (ML) method. The two specimens of A. japonica sp. nov. are shown with the sampling stations
and indicated in bold letters. The specimens from Sta. SJ3 and SJ4 were registered in DNA Data Bank of Japan (SJ3:
AB820365, SJ4: AB820366). Species retrieved from NCBI shown with their accession numbers. Numbers at nodes indicate NJ(Neighbor Joining)/ML bootstrap support values (only values higher than 50 are shown).

114

Y. Nakamura et al.

Fig. 7. Vertical distribution of temperature and salinity (A, D), biomass of Aulographis japonica (B, E) and proportion of thisspecies compared to the total zooplankton biomass sampled (C, F) at Sta. SJ1 and at Sta. SJ2 in the Sea of Japan during June
2011. T: temperature; S: salinity.

A. japonica, which was collected only from a cold watermass, i.e. JSPW, may also depend on water temperature.
Aulographis japonica showed a remarkable maximum
biomass in the mesopelagic zones at the two stations. Thistendency was also observed for the families Aulosphaeridae, Sagosphaeridae, Aulacanthidae and Coelodendridae
in the subarctic North Paciﬁc (Steinberg et al. 2008). Phaeodarians are presumed to feed upon detrital particles sinking from the epipelagic zone (Gowing 1986, 1989). It is
possibly better for them to inhabit zones as shallow as possible in the JSPW to efﬁciently obtain the organic matter
sinking from the upper layers, and this is probably one
reason for the highest abundance having occurred in theuppermost layer of the JSPW. Phaeodarians are hypothesized to be generalist feeders (Gowing 1986, 1989). Probably because of this generalist type of feeding, the present
species was able to maintain a certain level of biomass
despite the increasing depth. Considering its high relative
biomass, especially in deep waters, this species undoubtedly plays an important role in matter cycles in this area.
Despite its large contribution to total biomass, to ourknowledge this is the ﬁrst record of a phaeodarian species
in the Sea of Japan. Basic information such as the distribution or the ecology of phaeodarians still remains unknown.
The lack of taxonomic information on phaeodarians in the
Sea of Japan is probably one reason the abundant species
A. japonica was unknown until this study. Future studies
should focus on ecological aspects such as the life cycle
and regional distribution of this quantitatively important
species to better understand plankton ecology in the Sea ofJapan.
Acknowledgements
We thank the captains and crews of the T/S Oshoromaru and T/S Ushio-maru of Hokkaido University for
their assistance in sampling. We also thank the members of
the oceanic plankton group of Station Biologique deRoscoff for their kind technical advice. Appreciation is
also due to Ms. Yuka Mohri for molecular analysis and
Ms. Sarah Provost for advice about English writing. The
comments of Dr. Paulian Dumitrica, one anonymous re-A new phaeodarian species from the Sea of Japan

viewer and the editor also improved the manuscript. This
study was ﬁnancially supported by the Cooperative Research Project with Centre National de la Recherche Scientiﬁque (CNRS), “Morpho-molecular Diversity Assessmentof Ecologically, Evolutionary, and Geologically Relevant
Marine Plankton (Radiolaria)” by the Strategic International Research Cooperative Program hosted by the Japan
Science and Technology Agency (JST), and “Integrated
Research on Biodiversity of Interspecies Relationships” by
the National Museum of Nature and Science (A. Tuji).
References
Borgert A (1901) Die nordischen Tripyleen-Arten. Nord Plankton
15: 1–52.
Dogiel VA, Reshetnyak VV (1952) Some notes on Radiolaria of
the northwestern section of the Paciﬁc Ocean. Tr Zool Inst
Leningr, 3: 5–36. (in Russian)Felsenstein J (1985) Conﬁdence limits on phylogenies: anapproach using the bootstrap. Evolution 39: 783–791.
Gowing MM (1986) Trophic biology of phaeodarian radiolarians
and ﬂux of living radiolarians in the upper 200 m of the North
Paciﬁc central gyre. Deep-Sea Res 33: 655–674.
Gowing MM (1989) Abundance and feeding ecology of Antarctic
phaeodarian radiolarians. Mar Biol 103: 107–118.
Haeckel E (1887) Report on the Radiolaria collected by H.M.S.
Challenger during the years 1873–1876. Rep Sci Res Voyage
H.M.S. Challenger, Zoology 18: 1–1803.
Haecker V (1908) Tiefsee-Radiolarien. Wiss Ergebn dt TiefseeExped ʻValidiviaʼ 14: 1–706.
Horikoshi M, Nagata Y, Sato T, Handa N (1996) Oceans around
the Japanese Islands (Nature in Japan 7). Iwanami Shoten,
Tokyo, 316 pp. (in Japanese)
Immermann F (1904) Die Tripyleen Familie der Aulacanthiden.
Erg Plank-Exp Humboldt-Stiftung 3(1), 426 pp.
Jorgensen E (1907) Note sur les Radiolaires. Croisière Océanographique Belgica, Mer du Grönland (1905): 455–459.
Kawamura A (1989) Fast sinking mouth ring for closing Norpac
net. Nippon Suisan Gakk. 55: 1121. (in Japanese)
Kling S, Boltovskoy D (1999) Radiolaria Phaeodaria, South
Atlantic Zooplankton 1: 231–264.
Medlin L, Hille JE, Shawn S, Sogin ML (1988) The characterization of enzymatically ampliﬁed eukaryotic 16S like rRNAcoding regions. Gene 71: 491–499.

115

Meyer L (1933) Die geographische Verbreitung der tripyleen
Radiolarien des Südatlantischen Ozeans. Wiss Ergebn Dt
Atlant Exped ʻMeteorʼ 12: 122–198.
Nakayama T (2011) The great frontier of biology: diversity ofprotists. Bull Plankton Soc Jpn 58: 24–31. (in Japanese)
Nishimura S (1974) Origin and History of the Japan Sea: An
Approach from Biogeographic Standpoint, Tsukiji Shokan,
Tokyo. 227 pp. (in Japanese)Peters N (1928) Beiträge zur Planktonbevölkerung der WeddelSee. 4. Die tripyleen Radiolarien der Weddell-See. Int Revue
Ges Hydrobiol Hydrogr 21: 383–401.
Reshetnyak VV (1955) Vertical Distribution of Radiolarians in
the Kuril-Kamchatka Trench. Tr Zool In–ta Akad Nauk SSSR
21: 94–101. (in Russian)Reshetnyak VV (1966) The deep water radiolarian Phaeodaria in
the north west part of the Paciﬁc Ocean. Akademiya NaukSSSR Zoologicheskii Institut 94: 1–208. (in Russian)Schroeder O (1913) Die tripyleen Radiolarien (Phaeodarien).
Deutsch Sudpolar-Exped 1901–1903 14 (Zool 6): 113–215.
Steinberg DK, Cope JS, Wilson SE, Kobari T (2008) A comparison of mesopelagic mesozooplankton community structure in
the subtropical and subarctic North Paciﬁc Ocean. Deep-Sea
Res II 55: 1615–1635.
Sudo H (1986) A note on the Japan Sea Proper Water. Prog
Oceanogr, 17: 313–336.
Suzuki N, Aita Y (2011) Radiolaria: achievements and unresolved issues: taxonomy and cytology. Plankton Benthos Res
6: 69–91.
Takahashi K (1991) Radiolaria: ﬂux, ecology, and taxonomy in
the Paciﬁc and Atlantic. Ocean Biocoenosis Series 3, Woods
Hole Oceanographic Institution Press, Woods Hole, 303 pp.
Tamura K, Peterson D, Peterson N, Steker G, Nei M, Kumar S(2011) MEGA5: Molecular Evolutionary Genetics Analysis
using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731–2739.
Tibbs JF (1976) On some planktonic protozoa taken from thetrack of Drift Station ARLIS I, 1960–1961. Arctic Inst of
North America 20: 247–254.
Uda M (1934) The results of simultaneous oceanographical investigations in the Japan Sea and its adjacent waters in May
and June, 1932. J Imp Fish Exp Sta 5: 57–190. (in Japanese)
Wolfenden RN (1902) The plankton of the Faroe Channel and
Shetlands. Preliminary notes on some Radiolaria and Copepoda. J Mar Biol Ass UK 6: 344–372.