Bulletin of the Geological Survey of Japan, vol. 70 (1/2), p. 101–108, 2019

ArticleSummer surface water polycystine radiolariansin the eastern margin of the Japan Sea
Naoto Ishida1,*
Naoto Ishida (2019) Summer surface water polycystine radiolarians in the eastern margin of the Japan
Sea. Bull. Geol. Surv. Japan, vol. 70 (1/2), p. 101–108, 6 ﬁgs.
Abstract: In late August 2014, a living polycystine radiolarian assemblage was collected from thesurface waters off the shore of Sakata, Yamagata Prefecture, in the eastern margin of the Japan Sea.
The assemblage was dominated by the spumellarian Spongosphaera streptacantha, and included a
few individuals of Pseudocubus obeliscus and Tetrapyle octacantha. The intraspecific variation in S.
streptacantha observed in the main spine and spongiose layer was thought to reflect skeletal growth.
Morphometric analysis of the main spine and spongiose layer indicated that most individuals of S.
streptacantha were growing. On the sampling day, the surface water attained the annual maximum watertemperature and was strongly inﬂuenced by the Tsushima Warm Current. S. streptacantha inhabited thesummer surface water of this ocean area almost exclusively.
Keywords: living radiolarian assemblage, summer surface water, Spongosphaera streptacantha Haeckel,
Tsushima Warm Current, Japan Sea

1. Introduction

2. Oceanographic condition

The Japan Sea is a mid-latitude marginal sea enclosedby the Eurasian Continent, Japanese Islands, and Sakhalin(Fig. 1A). The surface water in the southeastern half of theJapan Sea is strongly inﬂuenced by the Tsushima Warm
Current (TWC), which ﬂows into the Japan Sea throughthe Tsushima Strait in the southwest and exits through the
Tsugaru and Soya (La Perouse) straits in the northeast.
Microplankton in the surface water of the TWC drift northand develop ontogenetically and heterogenetically under
the inﬂuence of the warm water, salinity, and nutriments.
Polycystine radiolarians are useful paleoenvironmental
indicators in the Japan Sea. Over the last 15 years, ourknowledge of radiolarians in the Japan Sea has increased
based on investigations using core sediments (e.g. Itaki,
2001; Itaki and Ikehara, 2003), surface sediments (e.g.
Itaki, 2003; Motoyama et al., 2016), and living material(e.g. Matsuoka et al., 2001; Itaki et al., 2003). This study
reports a living polycystine radiolarian assemblage in thehigh summer surface waters of the eastern margin of theJapan Sea. The assemblage provides useful informationon the skeletal growth of the radiolarian Spongosphaera
streptacantha and is very suggestive of the seasonalchange in surface-water radiolarians in the Japan Sea.

Figure 1A shows the surface currents in the Japan Sea
on the sampling day. After entering through the Tsushima
Strait, the TWC branched, meandered, and eddied in thesoutheast Japan Sea and ﬂowed toward the northeast
at less than 1 knot (Japan Coast Guard, 2014a). On thesampling day, one of the main currents of the TWC passed
through the Sado Strait and streamed along the west coastof Honshu, the main island of Japan. In 2014, the surface
water temperature at the sampling site reached the annual
maximum of 26–27 °C from August 25 to 27 (Japan Coast
Guard, 2014b).

1*

3. Sampling site and methods
The radiolarian assemblage investigated in this study
was collected by the research vessel Kaiyomaru No. 3(Kaiyo Engineering) in the early morning of August 26,
2014. The sampling was conducted at a site located about
65 km off the shore of Sakata, Yamagata Prefecture (38°59’44”N, 139°17’46”E; Fig. 1B). A 200-mm-diameter,
450-mm-long plankton net with a 72-µm mesh, wasused for the sampling. The net was towed by hand for
25 minutes at a depth of 10–15 m. The volume of waterﬁltered while sampling was not estimated.

Department of Social Systems and Civil Engineering, Graduate school of Engineering, Tottori University, Tottori 680–8550, Japan
Corresponding author: N. Ishida, Email: naoto-u.ac.jp− 101 −

Bulletin of the Geological Survey of Japan, vol. 70 (1/2), 2019

TTS

Eurasian
Continent

TobishimaIsland

km

60

120

SYS

Sampling site

Sado
Island

Japan

30˚N

Pacific
Ocean

38˚

A

138˚E

SakataAwashima
Island

ns

TGS

TSS

*

39˚N

tra
it

n
pa

a
Se

B

TWC

30

do
S

Ja

0

Sa

40˚

Sakhalinhu

140˚

Niigata

Ho

130˚E

139˚

B

Fig. 1 A) Geographical setting of the Japan Sea and surface currents on the sampling day (from the Japan
Meteorological Agency, 2014). Abbreviations are as follows: TWC, Tsushima Warm Current; TSS,
Tsushima Strait; TGS, Tsugaru Strait; SYS, Soya (La Perouse) Strait; TTS, Tatar Strait. The blacksquare indicates the area in B. B) Map showing the geography around the sampling site located off
Sakata, Yamagata Prefecture. The sampling site is indicated by the asterisk.

The sample was placed in ca. 10 % hydrogen peroxide
for several days to remove organic matter from theradiolarians. After rinsing with dilute hydrochloric acidto eliminate carbonates, the sample was sieved througha 41-µm mesh. The residue on the sieve was mounted
on glass slides using“Entellan New”mounting medium.
Radiolarians were observed and photographed bytransmitted light using a biological microscope.

4. Radiolarians
4. 1 Faunal composition
The sample contained 48 polycystine radiolarians, ofwhich 42 were Spongosphaera streptacantha Haeckel(87.5 %); a few Pseudocubus obeliscus Haeckel and
Tetrapyle octacantha Müller were also found. Figure 2
shows photomicrographs of the radiolarian species andindividuals from the sample.
4. 2 M orphologic variation of Spongosphaera streptacantha
Haeckel (1860) originally described the spumellarianspecies S. streptacantha. According to Kurihara andMatsuoka (2004), a typical specimen of S. streptacantha iscomposed of three main elements: the microsphere, main
spine, and spongiose layer (Fig. 2-1). The microsphereconsists of two concentric microspheres, the inner andouter microspheres, which are situated in the center of theskeleton. Six to nine main spines arise from the surfaceof the outer microsphere. A main spine has three distinct
ridges and grooves and is Y-shaped in cross-section.
Teeth-like apophyses are arrayed along the ridges of themain spines.
Wide intraspeciﬁc variation was recognised in S.
streptacantha in this assemblage. The microsphere andmain spine were observed in all specimens, whereas
the spongiose layer was sometimes absent. Figure 3
summarises the diameter of the outer microsphere, lengthof the main spine, and diameter of the spongiose layer of
37 specimens. The outer microsphere diameter ranged
from 35.4 to 41.7 (mean ± 1σ: 38.1 ± 1.6) µm and was
fairly uniform, while the length of the main spine anddiameter of the spongiose layer ranged widely (Fig. 3).
This study subdivided S. streptacantha into three classes
based on the developmental of the spongiose layer.
4. 2. 1 Morphotype-A
Nineteen specimens that lacked the spongiose layer
were classiﬁed into Morphotype-A. Figure 4 shows three
typical specimens of Morphotype-A. The main spines ofthis morphotype were shorter than those of Mophotypes-B
and -C (Fig. 3). The specimen in Figure 4-1 had a 44-µmlong main spine, which was the shortest in the study
assemblage. The main spines tapered toward the tips andwere fairly slender compared with those of the specimens− 102 −

Summer surface water radiolarians in the eastern margin of the Japan Sea (Ishida)1

ID: 332

3

4

5

microsphereouter microsphereinner microspherespongiose layer

main layer
innermost layer

main spine

100 µmfor all figures
Taxa (Photo No.)

Number of individuals

SPUMELLARIA
Spongosphaera streptacantha Haeckel (1)Tetrapyle octacantha Müller (4)421Taxa (Photo No.)

Number of individuals

NASSELLARIA
Pseudocubus obeliscus Haeckel (2, 3)
Nassellaria gen. et sp. indet. (5)41

Total number
Fig. 2 Transmitted light photomicrographs and list of polycystine radiolarians in the study assemblage. 1) Spongosphaera
streptacantha Haeckel. The specimen ID and skeletal characters are indicated. 2, 3) Pseudocubus obeliscus
Haeckel. 4) Tetrapyle octacantha Müller. 5) Nassellaria gen. et sp. indet.

µm

400

350

Morphotype-A

without spongiose layer

Morphotype-C
highly developed
Morphotype-B withspongioselayerwith weakly developed
spongiose layer

300ddiameter of outer microsphere250

length of main spine
length of main spine (broken)

200ddiameter of spongiose layer

150

100

50

0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37

Specimen ID

Fig. 3 The diameters of the outer microsphere, lengths of the main spine, and diameters of the spongiose layer of
37 specimens of Spongosphaera streptacantha in the study assemblage. S. streptacantha was subdivided into
Morphotypes-A, -B, and -C based on the development of the spongiose layer. The black diamond with “d”
indicates specimens with a delicate layer in the spongiose layer.
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Bulletin of the Geological Survey of Japan, vol. 70 (1/2), 2019

Fig. 4 Transmitted light photomicrographs of Spongosphaera streptacantha without a spongiose layer (Morphotype-A).
The specimen ID is indicated in each photograph. 1) A specimen with short main spines. The left main spine is
44 µm long. 2, 3a) Specimens with longer main spines. 3b) Close-up view of the main spine of the specimen
in 3a. Ridges and grooves are recognised only at the base and no serrated apophysis is seen. The base of themain spine is 3.4 µm wide.

in Figures 4-2 and 4-3.
The specimens shown in Figures 4-2 and 4-3 had main
spines 87 and 131 µm in length, respectively. Distinct
ridges and grooves were recognised only at the bases ofthese main spines (Fig. 4-3b). The main spine shown in
Figure 4-3b was 3.4 µm wide at the base. Although teethlike apophyses were visible along the edges of the main
spines of Morphotypes-B and -C, as described below,
none were observed in specimens of Morphotype-A (Fig.
4-3b).

than 150 µm were broken (Fig. 3). Figure 6-1b showsa close-up view of a main spine of Morphotype-C. The
maximum width of the main spine was 10.3 µm. Teeth-likeapophyses were visible at the edges of ridges. A delicate
layer was recognised only in two specimens with larger(>200 µm in diameter) spongiose layers (Fig. 3). The
specimen in Figure 6-2 possessed a delicate layer in partof the outer rim of the spongiose layer.

4. 2. 2 Morphotype-B
Seventeen individuals were classiﬁed as Morphotype-B,
which had a weakly developed spongiose layer (<120µm in diameter). Figure 5 shows three specimens ofMorphotype-B. The specimen shown in Figure 5-1 had afaint spongy network around the microsphere. The main
spines, 248 µm in length, tapered distally, like those in
Figure 4.
The specimens in Figures 5-2a and 5-3 had sparsely
developed spongiose layers. The main spines of these
specimens were over 300 µm in length; that of specimen
in Figure 5-3 was 402 µm long and was the longest in the
study assemblage. Distinct thin ridges and grooves wererecognised proximally and distally on the main spine in
Figure 5-2b. The maximum width of the main spine was
5.5 µm. Weakly developed teeth-like apophyses werevisible at the edges of the ridges and were connected withthe spongiose layer at the proximal part of the main spine.

5. 1 Intraspecific variation of Spongosphaera streptacantha
This study focused on the morphological variation of
S. streptacantha in terms of the diameter of the outermicrosphere, length of the main spine, and diameterof the spongiose layer. Previously, Kurihara andMatsuoka (2004) examined the skeletal development of
S. streptacantha in 19 specimens that had spongiose layers
ranging from 122.8 to 351.4 µm in diameter, which would
be classiﬁed into Morphotype-C of this study. By contrast,
as most specimens in the study assemblage were classiﬁed
into Morphotype-A or -B, this study can examine the earlystage of skeletal development of S. streptacantha.
All specimens had microspheres in the centers of theskeletons and the diameters were quite uniform (Fig. 3).
The microsphere is evidently formed in the initial stageof morphogenesis before the formation of the main spineand spongiose layer. Matsuoka (2017) shows a specimenof S. streptacantha with extremely short main spines, ca.
10 µm in length.
The lengths of main spines were distributed continuously
from 44 to 402 µm (Fig. 3). The width and structure of themain spine developed gradually in tandem with the length,
as is shown in Figures 4-3b, 5-2b, and 6-1b. This character
variation is considered to be a process of accretionary
skeletal growth.
The spongiose layer forms in the latter stage of skeletal

4. 2. 3 Morphotype-C
Six individuals were classiﬁed into Morphotype-C,
which had a large, dense developed spongiose layer(>120 µm in diameter). Three typical specimens ofMorphotype-C are shown in Figures 2-1, 6-1, and Fig.
6-2. The total length of the main spines of Morphotype-C
was unknown because most of the main spines longer

5. Discussion− 104 −

Summer surface water radiolarians in the eastern margin of the Japan Sea (Ishida)

Fig. 5 Transmitted light photomicrographs of Spongosphaera streptacantha with a weakly developed
spongiose layer (Morphotype-B). The specimen ID is indicated in each photograph. 1) A specimen
with slightly developed spongiose layer. The main spines of this specimen are thread-like and taper
at the top. The main spine is 248 µm long. 2a) A specimen with main spines with distinct ridges
and grooves. The spongiose layer is clearly observed. 2b) Close-up view of the main spine of thespecimen shown in 2a. Weakly developed serrated edges are seen. The maximum breadth was 5.5µm. 3) A specimen with a 402-µm-long main spine.

growth (Fig. 3). The delicate layer, which is in the
peripheral part of the spongiose layer, forms in the ﬁnal
phase of ontogenesis. Morphometric analyses of this study
and those of Kurihara and Matsuoka (2004) found that thedelicate layer develops in larger spongiose layers, over
200 µm in diameter.
The maximum size of the spongiose layer examined by
Kurihara and Matsuoka (2004) was 351 µm in diameter,while the largest one in this study was 267 µm. In
addition, no specimen in this study assemblage had a fully
developed delicate layer, as shown in Figure 9 of Kurihara
and Matsuoka (2004). Therefore, all the S. streptacantha
found in the study assemblage were immature individuals.

5. 2 Implication for radiolarian seasonal change in
the Japan Sea
Kurihara et al. (2007) noted that S. streptacantha ispresent in surface waters from late summer to early
autumn and prefers warmer water (>ca. 20 °C) based on
observations southwest of Sado Island, which is locatedca. 140 km southwest of the sampling site of this study.
For example, Matsuoka et al. (2001) and Kurihara andMatsuoka (2004, 2005) reported that P. obeliscus and S.
streptacantha were abundant in August and September.
In addition, Kurihara and Matsuoka (2007) collected an
assemblage dominated by three species, S. streptacantha,
P. obeliscus, and Pseudocubus sp. A, at 0–35 m depths on
September 28, 2005.

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Bulletin of the Geological Survey of Japan, vol. 70 (1/2), 2019

Fig. 6 Transmitted light photomicrographs of Spongosphaera streptacantha with highly developed
spongiose layers (Morphotype-C). The specimen ID is indicated in each photograph. 1a) A typical
specimen of Morphotype-C. The total length of main spine of this specimen is not known because
it was broken. 1b) Close-up view of the main spine of specimen of 1a. Distinct ridges and groove
are developed. Serrated apophyses align along the ridge lines. The maximum breadth was 10.3 µm.
2) A specimen with a weakly developed delicate layer in the outer periphery of the spongiose layer.

In comparison, S. streptacantha was absent from theassemblage collected from surface waters on May 20,
2002 off Sado Island (Itaki et al., 2003). A sample obtained
at 63–90 m depths on June 6, 2005, contained one possible
S. streptacantha (Kurihara et al., 2006). Each sample at
0–40 and 40–70 m depths on June 4, 2007 yielded one
individual (Kurihara et al., 2008). On June 7, 2010, only
one dead S. streptacantha was recovered at 100–200 m
depths (Kurihara and Matsuoka, 2011).
Except off Sado Island, only a few living S. streptacantha
in the Japan Sea have been studies. S. streptacantha was
not collected at a site northwest of Hokkaido in July
1999 (Itaki, 2003). Samples from depths shallower than
100 m in the Tsushima Strait on October 31, 2006 rarely
contained S. streptacantha (Itaki et al., 2010). Matsuzaki
et al. (2016) investigated the vertical distribution ofpolycystine radiolarians in the East China Sea southwestof the Tsushima Strait in late May 2008 and notedthat S. streptacantha was dominant at 20–50 m depths
characterised by high temperatures (>20 °C) and highchlorophyll αlevels.
This study obtained a polycystine radiolarian assemblage

composed mainly of S. streptacantha with a few P.
obeliscus. The faunal composition of the study assemblage
matches the assemblage reported in surface waters
around Sado Island in August and September. Although
S. streptacantha dominated the study assemblage, all theindividuals were immature and in the process of growing.
Therefore, S. streptacantha likely started proliferating justbefore the sampling and grows predominantly in the warm
summer surface waters under the strong inﬂuence of theTWC.

6. Summary
Living polycystine radiolarians were collected in lateAugust, 2014 from surface water at the eastern marginof the Japan Sea. This assemblage was dominated by
Spongosphaera streptacantha, with small numbers ofPseudocubus obeliscus and Tetrapyle octacantha. Manyof the S. streptacantha specimens were immature forms invarious stages of growth. S. streptacantha matured almost
exclusively in the warm summer surface water in thisocean area, which is strongly inﬂuenced by the Tsushima
Warm Current.

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Summer surface water radiolarians in the eastern margin of the Japan Sea (Ishida)

Acknowledgement
This study was conducted as part of the scientiﬁc
research program examining shallow gas hydrate in theJapan Sea. The author thanks Prof. Ryo Matsumoto of
Meiji University, the general manager of the research
programs. I also acknowledge Prof. Hideki Numanamiof Tokyo Kasei Gakuin University, Dr. Hitoshi Tomaru of
Chiba University, and the captain, crew, and scientists on
this cruise for their assistance with the sampling operation.
I also thank Dr. Isao Motoyama and Dr. Toshiyuki Kurihara
for their valuable suggestions, which helped to improve
the original manuscript. This study was partly supported
by JSPS KAKENHI Grant Number 16K05596.

References
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neuer Gattungen und Arten von lebenden Radiolariendes Mittelmeeres. Monatsberichte der Königlichen
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Itaki, T. (2003) Depth-related radiolarian assemblage inthe water column and surface sediments of the Japan
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Itaki, T. and Ikehara, K. (2003) Radiolarian biozonation
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Itaki, T., Matsuoka, A., Yoshida, K., Machidori, S.,
Shinzawa, M. and Todo, T. (2003) Late springradiolarian fauna in the surface water off Tassha,
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Japan Meteorological Agency (2014) Daily 50 m current,
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Kurihara, K. and Matsuoka, A. (2004) Shell structure

and morphologic variation in Spongosphaera
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Kurihara, T. and Matsuoka, A. (2005) Shell variability of
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Recieved December 19, 2017
Accepted January 18, 2019

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Bulletin of the Geological Survey of Japan, vol. 70 (1/2), 2019日本海東縁における夏季表層水の放散虫（ポリキスティナ）群集
石田直人

要 旨
2014年８月の後半，日本海東縁に位置する山形県酒田市沖の表層水から放散虫（ポリキスティナ）群集を採取した．この群集はSpongosphaera streptacanthaが大多数を占め，少数のPseudocubus obeliscus とTetrapyle octacanthaを伴う．S. streptacanthaにはmain spine やspongiose layerに種内変異が認められ，これは殻成長の過程を反映したものと考えられる．main spine とspongiose
layerの形態計測の結果は，この群集のS. streptacanthaの全てが成長途中の未成熟個体であることを示している．対馬暖流の強い影響下にあり，年最高水温に達していた採取地点の表層水では，S. streptacanthaが優占的に生育していたことが明らかとなった．

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