Molluscan response to early Pleistocene rapid
warming in the Sea of Japan
Akihisa Kitamura*
Hiroko Omote
Institute of Geosciences, Shizuoka University, Shizuoka 422-8529, Japan

Motoyoshi Oda
Department of Geoenvironmental Science, Tohoku University, Sendai 980-8578, Japan

ABSTRACT
Major changes occurred in the benthic molluscan fauna of the Sea of Japan continental shelfduring the transition from Pleistocene glacial to interglacial stages, owing to rapid warming associated with the inflow of the warm Tsushima Current. Molluscan associations representing thistransition occur in the lower Pleistocene Omma Formation in central Japan and suggest that
there were two patterns of faunal change. The first was when warm-water species migrated into
the Sea of Japan and lived along with cold-water species, accompanied by a northward shift in
species ranges. The second pattern involved the migration of warm-water mollusks shortly after
the local extinction of cold-water species. In the latter, it is possible that benthic molluscan communities with very low diversity and density existed temporarily and locally at inner shelf depths(<100 m) during the warming phase. Such a community has no modern analogue, but may haveresulted from a marine climate with a higher seasonality than occurs today. These findings showthat episodes of rapid warming have severe impacts on offshore benthic communities and molluscan species that include patterns not represented by modern faunal distributions.
Keywords: early Pleistocene, molluscan communities, Sea of Japan, obliquity, rapid warming.

INTRODUCTION
Understanding biotic responses to rapid climate change during the
Quaternary affords key insights for modeling and planning for possible
future human-induced climatic change (Overpeck et al., 1992; Valentine andJablonski, 1993; Faunmap Working Group, 1996; Roy et al., 1995, 1996;
Cronin and Raymo, 1997; Cannariato et al., 1999). These studies haveshown that species tend to respond in a Gleasonian model (Gleason, 1926)
to climatic fluctuations by migration. In this model it is assumed that species
respond in ecological time to environmental change in accordance with
their individual tolerance limits. Thus, migrations have resulted in significant changes in terrestrial and benthic marine faunas, often producing associations having no present-day analogues. These geologically temporary
faunal associations were likely caused by climatic conditions that differ
from the modern state (Webb et al., 1987; Overpeck et al., 1992). Increased
knowledge of biotic responses to rapid climate change during the Quaternary has been based largely on data from North America and Europe. In
contrast, few studies have addressed faunas in other temperate areas and therelatively monotonous offshore environment. In order to understand the
response of offshore fauna of the Northwest Pacific to environmental change,
we examined faunal changes among early Pleistocene marine mollusks
associated with rapid warmings within ten 41 k.y. obliquity driven climate
cycles in the Sea of Japan.

According to Ishiwatari et al. (1999), the alkenone-based sea-surface
temperature measured in sediment cores from the Oki Ridge shows asharp increase from 14 °C at 11.6 ka to 19 °C at 11.1 ka, as the warm
Tsushima Current began to flow into the Sea of Japan. The warming rate
was less than that predicted for future warming, but is very high for the
Quaternary of Japan. The rapid warming may have affected the shallow
water along the west coast of Honshu and thus may have strongly influenced organisms there. However, no study has been done on faunal change

EARLY PLEISTOCENE FOSSIL RECORD IN THE
SEA OF JAPANThe Tsushima Current, a branch of the warm Kuroshio Current, enters
the Sea of Japan through Tsushima Strait and makes its way northward
along the western coast of Honshu Island (Fig. 1). The current supplies
a large quantity of heat into the Sea of Japan. Therefore, the current
likely had a profound influence on the Quaternary paleoclimate andecosystem within and around the Sea of Japan (e.g., Oba et al., 1991).
*E-mail: seakita@ipc.shizuoka.ac.jp.
Geology; August 2000; v. 28; no. 8; p. 723–726; 3 figures.

Figure 1. Map of Sea of Japan and surrounding region, showing
location of Omma Formation.
723

Numbers of species
0

10

20

11

Figure 2. Stratigraphic distribution of mollusks in 11 6th-order (41 k.y.)depositional sequences of lower Pleistocene Omma Formation that accumulated during oxygen isotope stages 50 to 28.

25
28

29

30
31
10
Fig. 332
no fossils by secondary dissolution

34

35
8

36
7

37
no fossils by secondary dissolution

38

6
39

40

41

5
42
4

43

44
45

3
46

47
2

10

48
49
1

0

m

50
muddy fine grained to very fine grained sandstonewell-sorted fine-grained sandstonebasal shell bed
warm-water species
cold-water species
intermediate-temperature species
1-11: Depositional sequences
50-28: Oxygen isotope stages

724

during the past 12 k.y. on the continental shelf of the Sea of Japan, because
neither sediment nor fossil records for this period had been collected.
The Tsushima Current has flowed into the Sea of Japan during interglacial stages since oxygen isotope stage 49 (Kitamura et al., 1994).
Many early Pleistocene molluscan species still live in the Sea of Japan.
Thus, the pattern of faunal response to rapid warming during the early
Pleistocene transition from glacial to interglacial stages may be similar
to that of ca. 11 ka. We here present the stratigraphic distribution andabundance of environmentally sensitive benthic mollusks collected fromthe lower Pleistocene Omma Formation, a deposit that accumulated on
the continental shelf in the Sea of Japan.
The Omma Formation crops out around Kanazawa City along thewestern coast of central Japan (Fig. 1). The formation at its type section(exposed along the Saikawa River at Okuwa) has been divided into lower,
middle, and upper parts. The middle part is composed of 11 sixth-order(41 k.y.) depositional sequences that accumulated during oxygen isotope
stages 50 to 28 (Kitamura et al., 1994). These depositional sequences,
numbered 1 to 11 from oldest to youngest, consist mainly of inner shelf
sediments deposited in water depths <100 m (Kitamura et al., 1999). Depositional sequence 9 is not exposed at the type locality. Within a representative sequence, in situ molluscan faunal changes indicate that marine conditions changed from cold-water, upper-sublittoral to warm-water,lower-sublittoral, followed again by cold-water, upper-sublittoral conditions (Kitamura et al., 1994). We therefore examined the responses ofmolluscan species to rapid warming for 10 stage transitions (Fig. 2).
METHODS
The stratigraphic distribution and abundance of 99 molluscan species
collected from the middle part of the Omma Formation at the type section
was described by Kitamura (1991, 1995) and Kitamura et al. (1994, 1999)
as well as this study. There are two modes of occurrence of fossil mollusks
in the Omma Formation. The first is within a shell bed at the base of a depositional sequence, and the other consists of in situ mollusks in sandstone.
Mollusks in the basal shell bed were excluded from this study because they
were reworked from older deposits. All individuals of the in situ mollusks
in sandstone were identified and counted from a rectangular block of sandstone 1.0 m long parallel to strike and 0.5 m wide. The thickness of theblock ranged from 5 to 50 cm due to the uneven surface of the exposures.
Figure 2 shows the pattern of faunal change with numbers of species fromthe sandstone block.
Stratigraphic variations in the distribution of the mollusks indicate that
there were two patterns of faunal change in response to warming. The first isrepresented by the co-occurrence of warm- and cold-water species within asingle stratigraphic horizon. The second mode is when the stratigraphic distribution of both warm and cold faunas is separated by an interval barren ofmollusks. The barren zone has a maximum thickness of 30 cm (depositionalsequence 10), and its existence is significant for understanding biotic
responses to rapid warming. In order to learn more about the paleoenvironment, we examined the stratigraphic distribution of warm-water planktonic
foraminifera within the Omma sediments. Planktonic foraminifera werestudied from 25 1-cm-thick sediment samples from a 0.7-m-thick stratigraphic interval that includes the so-called barren horizon (Fig. 3). About 200
specimens of planktonic foraminifera were identified and counted per
sample from the >125 µm size fraction. The definition of warm- and coldwater species for both mollusks and planktonic foraminifera follows Kitamura et al. (1994) and Takemoto and Oda (1997), respectively. Warm and cold
assignments for 17 extinct molluscan species are based on the modern distribution of related living species. All extinct species, except for Pecten (Pecten)
GEOLOGY, August 2000

DISCUSSION
Communities situated on the geographic boundaries between warmand cold-water faunas commonly include mixtures of both elements (e.g.,
Jablonski and Valentine, 1990). Co-occurring warm- and cold-water mollusks are reported from Mutsu Bay and off Akita, at the modern northern
limit of warm-water mollusks in the Sea of Japan (Ishiyama, 1970;
Takayasu and Yunohara, 1977). If this boundary moved northward withwarming associated with the Tsushima Current, the molluscan faunalchange would be expressed as a pattern of cold-water species declining andwarm-water species increasing. Such a transition has been documented in
the rocky intertidal communities of Monterey Bay, California, where
species adapted to cooler conditions have declined while warm-adapted
species have increased with warming over the past 60 yr (Barry et al., 1995).
This pattern of faunal change is similar to that in depositional sequences 1,
3, 5, 6, 7, and 11, in which the offshore molluscan fauna contracted theirranges northward in response to inflow of the warm Tsushima Current into
the southern Sea of Japan.
There are no co-occurring cold- and warm-water mollusks in depositional sequences 8 or 10. It is noteworthy that intermediate-temperature
species are not present in the intervals between the horizon containing coldGEOLOGY, August 2000

Neogloboquadrina
pachyderma
sinistrally coiling form

Globigerinoides ruber

Globigerina bulloides

Cycladicama cumingi

Phacosoma japonicum

Barnea japonica

Cyclocardia ferruginea

Lucinoma annulata

Planktonic foraminifera

Tyasira tokunagai

Macoma nipponica

Ringicula doliaris

Yoldia notabilis

Acila insignis

Turritella saishuensis
saishuensis

columnFelaniella usta

Pandora pulchella

RESULTS
The appearance of warm-water mollusks occurs in the lower part ofthe muddy fine-grained to very fine grained sandstone within the Omma
depositional sequence (Figs. 2 and 3). An estimate of the time averaging offossil records is needed when attempting to infer biotic responses to rapid
climate change (Faunmap Working Group, 1996; Roy et al., 1996). According to Kitamura (1992), the mixing of skeletal elements was restricted
to a surface layer about 20 cm thick during deposition of the muddy finegrained to very fine grained sandstone. In depositional sequences 1, 3, 5, 6,
7, and 11 (correlated with oxygen isotope stage transitions 50 to 49, 46 to
45, 42 to 41, 40 to 39, 38 to 37, and 30 to 29), the faunal change is represented by the appearance together of warm- and cold-water species (Fig. 2)
in horizons 0.5 to 2 m thick. This co-occurrence of warm- and cold-watermollusks is not an artifact of postdepositional mixing. Thus, during inflowof the Tsushima Current into the Sea of Japan, warm-water species
appeared and became established, while many cold-water species disappeared, leaving few survivor species.
The number of cold-water species and individuals decreases upsection, and cold-water taxa are absent from depositional sequences 2, 4, 8, and
10 (Figs. 2 and 3). Warm-water species appear 10–30 cm above the disappearance horizon of cold-water species in depositional sequences 8 and 10(stage transitions 36 to 35 and 32 to 31) (Acila insignis in sequence 8; Yoldia
notabilis in sequence 10) (Fig. 3). These data imply that warm- and coldwater species did not always coexist. Both cold- and warm-water species
co-occur in thin horizons within depositional sequences 2 and 4 (stage transitions 48 to 47 and 44 to 43). The horizon in depositional sequence 2 isonly 6 cm thick but contains cold-water Turritella saishuensis saishuensis,
warm-water taxa Paphia schnelliana, and Zeuxis caelatus and theintermediate-temperature bivalve Macoma nipponica (Kitamura et al.,1999). In similar fashion, depositional sequence 4 contains a 20-cm-thickhorizon containing the cold-water bivalves Clinocardium fastosum andY. notabilis and the warm-water gastropod Onustus exutus. However,whereas individuals of M. nipponica are preserved in life position, the otherbivalves within these thin horizons are disarticulated. Considering theprevalence of disarticulated bivalves in these thin horizons, it is likely thatwarm-water species did not coexist with cold-water species during thewarming phases in depositional sequences 2, 4, 8, and 10. The stratigraphic
distribution of dominant planktonic foraminiferal species in depositionalsequence 10 is shown in Figure 3.

Molluscan fossils

Globigerina quinqueloba

byoritsuensis, are regarded as cold-water species. According to Amano andOhno (1988), P. byoritsuensis is regarded as a warm-water species.

20

0

cm

0

2 0 10

20

30

4 0

20

30 1 020

20 1 0 1 0 10 (%) 30 0 (%) 30 0 (%) 20 0 (%) 20

articulated shells

disarticulated shells

cold-water species

intermediate-temperature species

gastropods
warm-water species

Figure 3. Stratigraphic distribution of mollusks and selected planktonic
foraminifera in study section of depositional sequence 10 that accumulated during transition from oxygen isotope stages 32 to 31.

water species and the subsequent appearance of warm-water species indepositional sequences 8 and 10 (Fig. 3). The absence of molluscan fossils
within the barren zone may be due to sample size, but similar barren zones
are not present in depositional sequences 1, 3, 5, 6, 7, and 11, from whichmolluscan data were derived using the same sampling technique. Thus, it
seems possible that an environmental condition unfavorable for mollusks
temporarily prevailed during the warming phase.
As noted here, the mixing of fossil records was restricted to a surface
layer about 20 cm thick during deposition of the muddy fine-grained to veryfine grained sandstone. The stratigraphic position of the first warm-waterplanktonic foraminifera is 60 cm below the disappearance of cold-watermollusks in depositional sequence 10 (Fig. 3). Moreover, the occurrence ofthe dominant warm-water planktonic foraminifer, Globigerinoides ruber,suggests good preservation, because its test dissolves relatively easily(Hemleben et al., 1989). These data suggest that the appearance of warmwater planktonic foraminifera preceded the disappearance of cold-watermollusks. Thus, the local extinction of cold-water mollusks was caused bywarming due to the Tsushima Current. If the current transported the larvaeof warm-water mollusks into the study area, then environmental factors did
not allow them to survive. There is no significant change in the planktonic
foraminiferal fauna in the interval between the first appearance of warmwater planktonic foraminifera and the later appearance of warm-watermollusks, suggesting that no significant changes took place in factors suchas the sedimentation rate, productivity, salinity, or dissolved oxygen. Taken
together, these factors suggest that environmental conditions did not allow
offshore cold- and warm-water mollusks or intermediate-temperature mollusks to coexist in the study area.
The glacial-interglacial cycles of the early Pleistocene have an obliquity
cycle with a period of 41 k.y. The greater is Earth’s tilt, the more intense areseasons in both hemispheres; summers get hotter and winters colder. It issignificant that the volume of flow of the Tsushima Current is highly
seasonal. The maximum volume transported is 5.6 × 106 m3/s in September,or about 5–6 times as much as the minimum volume, which is transported
in winter (Isobe et al., 1994). The combination of high obliquity and seasonal volume changes implies high seasonality in bottom-water temperatures. This relationship is supported by the co-occurrence of warm-waterplanktonic foraminifera G. ruber and the cold-water, sinistrally coiling form725

of Neogloboquadrina pachyderma (Fig. 3). In addition, species living offshore tend to have narrow physiological tolerances (e.g., Jackson, 1974).
Thus, we infer that high seasonality resulted in an environment that was unsuitable for both offshore cold- and warm-water mollusks.
The last surviving cold-water mollusc was Y. notabilis, and the firstwarm-water immigrant was either Barnea japonica or Cycladicama
cumingi in depositional sequence 10 (Fig. 3). The stratigraphic position ofin situ B. japonica is about 10 cm below in situ C. cumingi, although thisdifference may be attributed to differences in their burrowing depths, because B. japonica may burrow as deep as 20 cm (Kondo, 1987). The relationship between reproductive cycle and thermal tolerance is unknown forthese species, and B. japonica is not known to exist in the modern Sea ofJapan. Because of this, our inference of unsuitable seasonality based on thegeographic distribution of Y. notabilis and C. cumingi remains tentative.
The bivalve Y. notabilis is reported from Akkeshi to Ishinomaki along thenorthwestern Pacific (eastern) shelf of the Japanese Islands (Nakaoka,1989) (Fig. 1), where it is absent from water masses with a maximum mean
monthly temperature >20 °C. However, the distribution of C. cumingi extends through Tsugaru Strait to the northern Sanriku coast, and is influenced
by the Tsugaru Current, a branch of the warm Tsushima Current (Ishiyama,1973) (Fig. 1). On the basis of water temperature alone, the Sanriku coast is
substantially north of the northern limit of C. cumingi. Mean bottom-watertemperatures for March and September in this area are 6 °C and 20 °C, respectively, and these are the temperature limits for C. cumingi. Therefore,
the absence of Y. notabilis and C. cumingi implies winter temperatures
lower than 6 °C and summer temperatures higher than 20 °C. Such high seasonality does not occur on the modern-day continental shelf around theJapanese Islands. In summary, a marine climate having no modern analogues in the Sea of Japan briefly prevailed on the continental shelf during
warming associated with inflow of the warm Tsushima Current into the Sea
of Japan and resulted in benthic communities with very low density anddiversity of mollusks. These fossil patterns indicate that rapid climate transitions have a severe impact on offshore communities and a Gleasonianmodel is valid to predict the effects of rapid warming on marine communities in this sector of the northwest Pacific.
ACKNOWLEDGMENTS
This study was funded by a grant-in-aid from the Ministry of Education,
Science and Culture of Japan (08454150 and 10304040) and the Saneyoshi scholarship foundation.
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