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Transactions and Proceedingsof thePalaeontological Society of Japan

New SeriesNo. 182

June 30, 1996

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Trans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.413-418, 4 Figs., June 30, 1996
© by the Palaeontological Society of Japan 1996

1

1008

1

Shako, a new Miocene stomatopod Crustacea from JapanHIROAKI KARASAWA
Mizunami Fossil Museum, Yamanouchi, Akeyo, Mizunami, Gifu Prefecture, 509-61 Japan
Received 18 August 1995; Revised manuscript accepted 8 March 1996
Abstract. The monotypic genus Shako (Crustacea, Stomatopoda) is erected with S. tomidai sp. nov. from
the Miocene Ayugawa and Mizunami Groups (Lower Miocene) of Central Japan. This is the second
record of the Stomatopoda from Cenozoic deposits of Japan. It appears that S. tomidai preferred abrackish water environment
Key words: Crustacea, Stomatopoda, Shako, Miocene, Japan

Introduction
The order Stomatopoda Latreille, 1817 (Crustacea) contains
15 extant families, the Carboniferous Tyrannophontidae
Schram, 1969 and the Jurassic-Cretaceous family Sculdidae
Dames, 1886 (Shram, 1986; Muller, 1994). Fossil records of
the Stomatopoda are rare in Mesozoic and Cenozoic
deposits throughout the world. In the review of fossil
records by Holthuis and Manning (1969; R541), four extinct
sculdid and four extant squillid genera (Le. Gonodactylus
Berthold, 1827, Hemisquil/a Hansen, 1985, Squil/a Fabricius,1787, Chloridella Miers, 1880=C/orida Eydoux and Souleyet,1842) are recorded. According to Manning's 1980 classification, Gonodactylus belongs to the family Gonodactylidae
Giesbrecht, 1910 and Hemisquilla to the family Hemisquillidae
Manning, 1980.
Secretan (1975) assigned Squil/a antiqua Munster, 1842,
from the Upper Eocene of Italy to Lysiosquil/a Dana, 1852
(Lysiosquillidae), while Squil/a wetherelli Woodward, 1879
from the Eocene London Clay of England was assigned to
the genus Bathysquil/a Manning, 1963 (Bathysquillidae) byQuayle (1987). Schram (1968) erected a new monotypic
genus, Paleosquil/a (Gonodactylidae), from the Upper
Cretaceous of Colombia, South America. Forster (1982)
described three new species, Squil/a hollandi (Squillidae) and? Pseudosquil/a wulfi (Pseudosquillidae), from the Upper
Eocene of North Germany, and Lysiosquilla nkporoensis fromthe Upper Cretaceous of Nigeria. Yun (1985) gave detailed
descriptions of five fossil species in three genera, Squil/a,
Leesquil/a Yun, 1985 and Pohsquil/a Yun, 1985, of the Squillidae from the Miocene of Korea. Karasawa and Nakagawa(1992) recorded Oratosquilla ? sp. (Squillidae) from the
Miocene Shimo Formation of Fukui Prefecture. Thus,
eleven genera in five extant families have been recognized
as fossils.
The purpose of this paper is to describe a new genus andspecies of squillid from the Ayugawa and Mizunami Groupsof Central Japan, and discuss the paleoecology of thisspecies based on the associated decapod fauna.
Systematics
Family Squillidae Latreille, 1803
Genus Shako gen. nov.

Type species.-Shako tomidai sp. nov. by monotypy;masculine gender; Early Miocene; Japan.
Derivation of name.-The name is derived from theJapanese word for stomatopod.
Diagnosis.-Moderate sized squillid, total length less than
150 mm. Eye small, cornea bilobed, stalk long. Carapace
narrowed anteriorly, without median carina; cervical groove
distinct; anterolateral angles spined; posterolateral margins'strongly convex. Last three thoracic somites with welldeveloped submedian and intermediate carinae; lateralprocess of 5th thoracic somite developed as single, narrow,gently curved spine, directed anterolaterally; lateral processes of next two somites posterolaterally rounded. Abdomenwith submedian, intermediate, lateral and marginal carinae,
4th and 5th somites with median carinule. Telson inflated,slightly broader than long, tapering posteriorly, with dorsal
median carina and 6 small, triangular marginal teeth; submedians with fixed apices; intermediate denticles in a sharp
oblique, slightly convex row; dorsal surface of telson finely
granulated. Dactylus of raptorial claw with 5 teeth on inner
margin; outer margin of dactylus sinuate; inner margin of
propodus pectinate; dorsal ridge of carpus unarmed.
Discussion.-This new genus is assigned to the Squillidaeby having a carinate dorsal body, a pectinate inner margin of
the propodus, and the telson with a distinct median carina
and 18 intermediate denticles, although the ocular scales,
the propodi of 3rd and 4th thoracic appendages and thebasal prolongation of the uropod are unknown.
Manning (1968) indicated that there were four genericgroups within the Squillidae. Shako belongs to his thirdgroup in that the lateral process of the 5th thoracic somite is414

Hiroaki Karasawa

2

Figure 1. Shako tomidai gen. et sp. nov., MFM39013 (holotype). 1. x 1.5, dorsal view of anterior part of body.
2. x 2.0, dorsal view of eye and anterior part of carapace. 3, 4. x 1.5, lateral view. 5. x 1.5, dorsal view of posterior
part of body.

1008.

New Miocene stomatopod Crustacea

developed as a single spine, the eye is small, and thecarapace and an inflated abdomen have a reduced complement of carinae. Shako differs from C/orida Eydoux andSouleyet, 1842, a typical genus of the group, in having abroad telson with dorsal spines and tubercles, and thesubmedian teeth without movable apices. Shako appears
to be related to the Recent genera C/oridopsis Manning,
1968, and Lenisquil/a Manning, 1977, in structure of thelateral process of the 5th thoracic somite and in the telsonwith fixed apices. The new genus differs from C/oridopsis in
the lack of a median carina on the carapace, the shape ofthe lateral process of the 6th and 7th thoracic somites,
presence of median carinules on the 4th and 5th abdominal
somites, and the dorsal surface of the telson. Presence ofmedian carinules on the 4th and 5th abdominal somites andthe prelateral lobe of the telson, and short marginal teeth of
the telson readily distinguish Shako from Lenisquil/a.
Shako appears to show an affinity with the Korean
Miocene genus, Leesquil/a Yun, 1985 in the shape of thelateral processes of the 5th-7th thoracic somites, but differsin having a small eye, and lacking a median carina on the
carapace and abdominal somites. The lateral process of
the 5th thoracic somite in Shako is a narrow, gently curved
spine, whilst in Leesquil/a it is a large, acute spine strongly
directed anteriorly. The dactylus of the raptorial claw in

Id

415

Shako has five teeth, whereas in Leesquilla it has four.
Short, triangular marginal teeth of the telson readily distinguish Shako from Leesquil/a and the second Korean
Miocene genus Pohsquil/a Yun, 1985.

Shako tomidai sp. nov.
Figures 1-4
Material examined.-MFM39013 (holotype), a road cut of
Nishino, Ayugawa, Tsuchiyama-cho, Koga-gun, Shiga Prefecture (34°56'32"N, 136°19'24"E), collected by M. Kametaka; Sendai Sandstone Mudstone Member, Tsuchiyama
Formation, Ayugawa Group (Lower Miocene, Zones N7 -N8of Blow's scale by Yoshida, 1992)-MFM9042 (paratype),
Loc. 36 of Karasawa (1991), dry riverbed southeast of
Shomasamahora, Tsukiyoshi, Akeyo-cho, Mizunami City,
Gifu Prefecture (35°22'42"N, 13T14'E), collected by T.
Kaede; Tsukiyoshi Member, Akeyo Formation, Mizunami
Group.
Repository.-AII type specimens are housed in the
Mizunami Fossil Museum, Yamanouchi, Akeyo-cho,
Mizunami, Gifu, 509-61 Japan.
Derivation of name.-In honor of my friend, Dr. Susumu
Tomida (Chukyo Gakuin University, Gifu), a molluscan

It

id

ic

sd -~'~Ii<:li"-

sc

5

6

c

m

'\

pc

-lern
Figure 2. Shako tomidai gen. et sp. nov., MFM39013 (holotype). Explanation: 5-8, fifth to eighth thoracic
somites· I-VI first to sixth abdominal somites; as, antennal scale; bs, basal segment of uropod; C, carapace; c,
carpus; ,cg, 'cervical groove; d, dactylus; gg, gastric groove; ic, intermediate carina; id, intermedi~te denticl~ ;it, intermediate tooth; Ic, lateral carina; Id, lateral denticle; It, lateral tooth; Ip5, lateral process of fifth thoraCIC
somite; m, merus; mc, marginal carina; mdc, median carina; mdcr, median carinule; 0, eye; P, pereiopods; p,
propodus; pc, pectinations; pi, prelateral lobe; Rc, Raptorial claw; sc, submedian carina; sd, submedian denticle; st, submedian tooth; T, telson.

II

4 16

Hiroaki Karasawa

Figure 3. Shako tomidai gen. et sp. nov. 1a, b, MFM9042 (paratype), X 1.5, a : dorsal view of thoracic andabdominal somites, b : dorsal view of telson. 2. MFM39013 (holotype), x 2.0, dorsal view of telson.
paleontologist, who studied decapod fossils from theMizunami Group in his early years.
Diagnosis.-As for genus.
Description.- Size moderate, total length less than about
150 mm. Eye small, cornea bilobed and slightly broader
than stalk, stalk length about 0.75 times as long as eye
length. Antennal scale less than half as long as carapace.
Antennular somite poorly preserved. Ocular scales notpreserved. Rostral plate broken.
Carapace narrowed anteriorly. Anterior margins of carapace concave. Anterolateral spine weak, not extending tobase of rostral plate. Median carina lacking, intermediatecarinae not extending to cervical groove, lateral and marginal
carinae well developed. Posterolateral margins strongly
convex.
Lateral process of 5th thoracic somite developed as
single, narrow, gently curved spine, directed anterolaterally,
posterior margin gently convex. Lateral processes of 6th
and 7th somites posterolaterally rounded. Somites
decreasing in size anteriorly with well developed, unarmed

submedian and intermediate carinae, and without mediancarina.
Abdomen strongly carinate, increasing in width posteriorly,
but 6th somite narrower than 5th. Articulated anterolateralplates of abdomen absent. Submedian, intermediate, lateraland marginal carinae distinct ; submedian carinae slightly
divergent posteriorly on 2nd to 5th somites and inflated,slightly convergent on 6th somite; 4th and 5th somites withinterrupted median carinule. None of all abdominal spines
armed posteriorly.
Telson longitudinally convex, slightly broader than long,tapering posteriorly. Lateral, intermediate and submedianteeth small, triangular. Submedians with fixed apices. All
marginal teeth inflated at the base. Two lateral, 18 intermediate and 6 submedian denticles small, rounded ; intermediate denticles in a sharp oblique, slightly convex row. Dorsal
surface finely granulated without radial ornamentations,strong median carina well developed without distal spine.
Raptorial claw large. Dactylus slender, about 0.75 times
as long as carapace length, with 5 teeth decreasing in size

1008.

New Miocene stomatopod Crustacea

417

mizunamiensis Itoigawa and Vicaryella ishiiana Yokoyama

were found at the decapod-bearing localities (Karasawa,1991). Thus, it appears that S. tomidai preferred to inhabit amuddy bottom in the intertidal zone under the influence of
low-salinity water.

Acknowledgments
I thank Dr. R.B. Manning (Smithsonian Institution, Washington, D.C.) for critically reading the manuscript, Prof. J. Itoigawa (Sugiyama Jogakuen University) for advising me on thegeneric name, and Mr. M. Kametaka (Nagoya University) and
Mr. T. Kaede (Inazawa City) for offering their fossil
stomatopod specimens.

References cited
Berthold, A.A., 1827: Latreille's NatUrliche Familien desThierreichs, aus dem Franzosischen mit Anmerkungen
und Zusiitzen, x+606 p. Weimar.

Dames, W.B., 1886: Ueber einige Crustaceen aus den
Kreideablagerungen des Libanon. Zeitschrift derdeutschen geologischen Gesel/schaft, vol. 38, p.551575.
Dana, J.D., 1852: Crustacea. Part 1. In, United States
Exploring Expedition during the Years 1838, 1839, 1840,
1841, 1842 under the Command of Charles Wilkes, U.S.
N., vol. 13, p.1-685.
Eydoux, A.M. and Souleyet, L., 1842: Crustaces. In, Voyage autour du monde executee pendant les annees
1836 et 1837 sur la corvette La Bonite commandee par
M. Vaillant, Capitaine de Vaisseau, Zoologie, vol. 1, p.

Figure 4.

Reconstruction of Shako tomidai gen. et sp. nov.

219-272.
Fabricius, J.C., 1787: Mantissa Insectorum sistens eorum
species nper detectas adjectis characteribus genericis,
differentiis specificis, emendationibus, observationibus,

proximally on inner margin, outer margin of dactylus sinuate.
Propodus with fine pectinations on inner margin. Carpus
bearing 4 small, bluntly triangular teeth on outer margin,
dorsal ridge of carpus unarmed.
Paleoeco/ogy.-The holotype specimen was collectedfrom mudstone of the Ayugawa Group of Shiga Prefecture,associated with a pelecypod, Trapezium modiolaeforme
Oyama and Saka (Tanaka and Kimura, per. com.). T.
modiolaeforme is found in the Cyclina- Vicarya and Vicaryellabacula-Cyclina assemblages which represent a shallow
estuarine environment from the Ayugawa Group (Shibata,1975).
Karasawa (1991 ; 1993) reported six species of decapod
from the Mizunami Group of the fossil-bearing locality within
Mizunami City, Gifu Prefecture. The decapod assemblage
is dominated by Upogebia mizunamiensis Karasawa andLaurentiella imaizumii Karasawa. Associated with them,
Laomedia praeastacina Karasawa, Scylla ozawai Glaessner,
Miosesarma japonicum Karasawa, and Varuninae gen. et sp.
indet. occur rarely.
The depositional environment of the localities was interpreted as an intertidal zone of muddy bottom (Karasawa,1991). The brackish-water molluscs Cyclina japonica
Kamada, Vicarya yokoyamai Takeyama, Batil/aria

vol. 1, ixx+348 p. Hafniae.
Forster, R., 1982: Heuschreckenkrebse (Crustacea,
Stomatopoda) aus dem Alttertiar von Helmstedt undHadorf (Niedersachsen) und der Oberkreide von Nigeria.
Neues Jahrbuch fiir Geologie und Paliiontologie, Monatshefte, Heft. 6, 1982, p.321-335.
Giesbrecht, W., 1910: Stomatopoden. Erster Theil. Fauna
und Flora des Goffes von Neapel, Monographie, vol. 33,

239 p. Berlin.
Hansen, H.J., 1895: Isopoden, Cumaceen und
Stomatopoden der Plankton-Expedition. Ergebnisse
Plankton-Expedition der Humboldt-Stiftung, vol. 2, no.
Gc, p.1-105.
Holthuis, L.B. and Manning, R.B., 1969: Stomatopoda, In,
Moore, R.C. ed., Treatise on Invertebrate Paleontology,
Part R, Arthropoda (4), p. R535-552. Geological Society of America and University of Kansas Press.
Itoigawa, J., 1980: Geology of the Mizunami district, central
Japan. Monograph of the Mizunami Fossil Museum,no. 1, 50 p. (in Japanese)
Karasawa, H., 1991: Decapod crustaceans from the
Miocene Mizunami Group, central Japan. Part 3.
Decapod crustacean assemblage and paleoecology,
with description of two species. Bul/etin of the
Mizunami Fossil Museum, no. 18, p.1-18.
Karasawa, H., 1993: Cenozoic decapod Crustacea from

Hiroaki Karasawa

418

southwest Japan. Bulletin of the Mizunami Fossil
Museum, no. 20, p.1-92.
Karasawa, H. and Nakagawa, T., 1992: Miocene crustaceans from Fukui and Ishikawa Prefectures, central
Japan. Bulletin of the Japan Sea Research InstituteKanazawa University, no. 24, p.1-18. (in Japanese withEnglish abstract)
Latreille, P.A., 1803: Histoire naturelle, generale et particuliere, des crustaces et des insectes. vol. 3, 468 p.
Paris.
Latreille, P.A., 1817: Les crustaces, les arachnides et les
insectes. In, Cuvier, G., Le regne animal distribue d'apres son organisation, pour servir de base a I'histoire
naturelle des animaux et d'introduction
i'anatomie
comparee, edition 1, vol. 3, p. i-xxix+1-653. Paris.
Manning, R.B., 1963: Preliminary revision of the genera
Pseudosquilla and Lysiosquilla with descriptions of six
new genera (Crustacea, Stomatopoda). Bulletin ofMarine Science, vol. 13, p.308-328.
Manning, R.B., 1968: A revision of the family Squillidae(Crustacea, Stomatopoda), with the description of eight
new genera. Bulletin of Marine Science, vol. 18, p. 105142.
Manning, R.B., 1977: Preliminary accounts of five newgenera of stomatopod crustaceans. Proceedings ofthe Biological Society of Washington, vol. 90, p.420423.
Manning, R.B., 1980: The superfamilies, families, and genera of recent stomatopod Crustacea, with diagnoses ofsix new families. Proceedings of the Biological Societyof Washington, vol. 93, p.362-372.
Miers, E.J., 1880: On the Squillidae. The Annals andMagazine of Natural History, series 5, vol. 5, p. 1-30 and
108-127.
MOiler, H.G., 1994: World Catalogue and Bibliography of theaRecent Stomatopoda, 288 p. Wissenschaftlicher Verlag,
Wetzlar.
MOnster, G. Graf zu, 1842: Beschreibung drei neuer Arten
Crustacizen. Beitrtige zur Petrefactenkunde, vol. 5, p.
76-77.
Quayle, W.J., 1987: English Eocene Crustacea (lobsters
and stomatopod). Palaeontology, vol. 30, p.581-612.
Schram, F.R., 1968: Paleosquilla gen. nov.-A stomatopod(Crustacea) from the Cretaceous of Colombia. Journalof Paleontology, vol. 42, p. 1297-130t
Schram, F.R., 1969: Some middle Pennsylvanian Hoplocarida and their phylogenetic significance. Fieldiana:
Geology, vol. 12, p.235-289.
Schram, F.R., 1986: Crustacea, 606 p. Oxford University
Press, New York.
Shibata, H., 1975: Molluscan paleoecology of the Miocene
First Setouchi Series in the eastern part of the Setouchi
Geologic Province, Japan. Bulletin of the Mizunami
Fossil Museum, no. 5, p.23-11O.
Secretan, S., 1975: Les Crustaces du Monte Bolca. In,
Stovoi e Richerche sui Giacinenti Terziare di Bolca, vol.
2, p. 315-338. Museo Civico di Storia Naturele di
Verona.
Woodward, H., 1879: Contributions to the knowledge offossil Crustacea. Quarterly Journal of the GeologicalSociety of London, vol. 35, p.549-55t
Yoshida, S., 1992: Geologic development of the Setouchi
Geologic Province since Early Miocene-with specialreference to the First and Second Setouchi Inland Seatimes. Bulletin of the Geological Survey of Japan, vol.
43, p.43-67. (in Japanese with English abstract)
Yun, H., 1985: Some fossil Squillidae (Stomatopoda) fromthe Pohang Tertiary basin, Korea. Journal of the
Paleontological Society of Korea, vol. 1, p.19-31.

Trans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp. 419-431, 7 Figs., June 30, 1996

© by the Palaeontological Society of Japan 1996

/1009/ Larval paleoecology of the late Pleistocene naticid
gastropod Cryptonatica with two protoconch types
from the Oga Peninsula, northern Japan
SHIN'ICHI NISHINOSONO
Geological Institute, University of Tokyo, Hongo 7-3-1, Tokyo, 113 Japan
Present address: Nuclear Safety Bureau, Science and Technology Agency, Kasumigaseki 2-2-1, Tokyo, 100 Japan

Received 13 September 1995; Revised manuscript accepted 15 February 1996
Abstract. Gastropod fossils from the upper Pleistocene marine sequence in the Oga Peninsula, northern
Japan, were analyzed, with special reference to the larval paleoecology and taxonomic relationships of
Cryptonatica with two different protoconch types. The frequency of warm-water species increases
towards the top of the section, with a gradual decrease in the frequency of cold-water species, suggesting
gradual warming of the ambient sea water under the influence of the Tsushima currents from the south
during 100-134 Ka. Available data on the relationship between protoconch morphology and mode of
development in extant naticids strongly suggest that the two morphotypes of Cryptonatica, whose
teleoconch morphologies are comparable to C. andoi, probably underwent different modes of development, i.e. planktotrophy for the type with a smaller protoconch (S-type) and non-planktotrophy for the typewith a larger protoconch (L-type). The taxonomic relationships of the two morphotypes of Cryptonatica
can be interpreted as closely allied different species (cryptic species) rather than dimorphs of a single
species with different developmental modes (poecilogony), since the latter phenomenon is quite rare inmodern marine invertebrates. Comparison with type and figured specimens of C. andoi and related
species of the same genus shows that specimens of S-type are referable to C. andoi (Nomura), while thoseof L-type may belong to a new species; here I provisionally treat them under C. sp. aft. C. andoi.
According to this interpretation, the transition of developmental modes from non-planktotrophy to planktotrophy may have occurred in association with a speciation event of the "Cryptonatica andoi" lineage
at least before late Pleistocene time.
Key words: Cryptonatica, Naticidae, Pleistocene, Oga area, larval ecology, cryptic species, evolution

Introduction
A major goal of paleontology is to understand how thebiological characteristics of fossil organisms have influenced
their success on the earth (Em let, 1989). Many marine
invertebrates undergo a larval stage during a limited interval
between hatching and metamorphosis. Developmental
mode may influence autecology, modes of selection, andrates of speciation and extinction 0Nary and Raff, 1991).
The excellent fossil record of marine molluscs allows us to
examine the life history and the tempo and mode of morphological evolution by the comparison of fossil remains withrelated living representatives.
Gastropods secrete a protoconch shell that formed during
embryogenesis and/or during the post-hatching larval stage
before metamorphosis. Since the early studies of Thorson(1950), Shuto (1974) and Jablonski and Lutz (1980) on therelationship between protoconch morphology and mode of

development in extant species, microscopic studies of the
protoconch have become one of the useful approaches tothe study of larval ecology and paleoecology of gastropods.
Until now, it has been generally thought that larval ecology
is stable throughout a given gastropod lineage. Jablonski(1986) emphasized the species-level invariability of the modeof development in gastropods. Protoconch morphology has
been frequently utilized as a reliable basis for phylogenetic
reconstruction. For example, two turrid genera, Guraleus
and Antiguraleus, are distinguished based on differences inprotoconch morphology that reflect larval ecological differences (Shuto, 1994). The idea that larval ecology is invariant at the species level may influence or be influenced by
the definition of taxa. This can lead to circular arguments.
On the other hand, some taxonomists have made allowancefor polarity of changes in protoconch morphology. Bouchet(1990) suggested the possibility that protoconch morphology
in the Turridae exhibits polarity from multispiral type toShin'ichi Nishinosono

420

pauspiral type reflecting planktotrophy and non- planktotrophy respectively. Nevertheless, the relationship between
developmental modes and phylogeny in gastropods has not
yet been sufficiently elucidated.
The family Naticidae possess unique egg masses called
egg collars (e.g. Giglioli, 1955 ; Amio, 1955). The larval
ecology in some species of this family has been studied

experimentally (e.g. Amio, 1955). Furthermore, fossils of thisfamily are found abundantly in marine Cenozoic strata in thenorthern Pacific region including Japan (Marincovich, 1977 ;Majima, 1989). In this study, larval ecology and taxonomy ofa naticid, "Cryptonatica andoi Nomura, 1935" with two
protoconch morphotypes are examined based on upper
Pleistocene and Recent specimens. The purpose of thisKatanishi F. ~Anden F.

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Sea of Japan

0Marine molluscs
0- b Brackish and fresh-water bivalves
0- t Impression fossils
Xsilt

No molluscs

conglomerate

Figure 1. Geological column of the upper Pleistocene sequence exposed along the Anden coast, north of the
Oga Peninsula, northern Japan (arrow on index map), showing the stratigraphic positions of fossil localities.

1009.

Larval paleoecology of late Pleistocene Cryptonatica

paper is to demonstrate how developmental mode in gastropods is affected by paleoenvironmental change and to
examine the stability of developmental modes within a lineage.
Materials and methods
Geological settings of fossil- bearing strata
Naticid fossils from the late Pleistocene marine strata
exposed at the Anden Coast, Oga City, were used for the
study of change in larval paleoecology (Figure 1). The strata
are divided into the Wakimoto, the Shibikawa, the Anden,
and the Katanishi Formation based on lithostratigraphy (Kitazato, 1975). The Shibikawa Formation overlies the massive mudstone of the Wakimoto Formation. It attains about
120 m in thickness in the studied section. Two sedimentary
cycles are recognized in the Shibikawa Formation : coarse
sand or granule- sized gravel beds grading upwards into
medium to fine sand and silt and terminating in a lignite bed.
The age of the lignite bed in the upper cycle is 103- 123 Ka
based on fission track analysis of an enclosed volcanic ash
layer (Aso- 3) (Okaguchi, 1978 ; Nagatomo, 1990; Matsumoto et a/., 1991).
The Anden Formation clinounconformably covers the
Shibikawa Formation. It attains about 10 m in thickness andconsists of sand and sandy silt with an intercalation ofmassive pink tuff. The pink tuff has been identified as the
Toya Tuff, which has fission track ages of 103-134 Ka (Takashima et a/., 1992). The Katanishi Formation, more than 15
m thick, conformably covers the Anden Formation. It consists mainly of alternating fine and modium sand beds with ashell bed containing disarticulated G/ycymeris at the base.
It also contains a tuff correlated with the Aso- 4 Tuff (86- 90
Ka fission track age, Oba, 1991).
In both Shibikawa and Anden Formations, the lower andmiddle parts of the cycle are rich in shallow- marine invertebrate fossils (molluscs, brachiopods and echinoids), while theuppermost part contains brackish to freshwater bivalves(ostreids and corbiculids) and water nuts (Trapa sp.). Molluscan shell beds are intercalated at two horizons in the
Shibikawa Formation; I will refer to them as the lower andupper shell beds. Recent studies on the sequence andoxygen isotope stratigraphy in combination with the faunalanalysis have suggested that lithologic and faunal changes
in the upper Pleistocene sequence in the Oga Peninsula

Table 1.

42 1

were controlled by global glacial eustatic sea- level changes(Matoba, 1992 ; Shirai, 1995MS).
Materials
5,000 cm 3 of fossil bearing sediment was collected ateach of the ten horizons in the Shibikawa Formation [ 7horizons in the lower shell beds (S- 1 to S- 7) and 3 horizonsin the upper shell beds (S- 8 to S-10)J and each of the sevenhorizons in the Anden Formation (A-1 ~A- 7) (Figure 1). Eachsediment sample was sieved with a 2 mm mesh screen, andgastropod fossils in the residue were picked and identified.
A total of 1640 speCimens belonging to 75 species wereidetified (see Appendix I).

Diameter of the firsthalf volutionadiameterFigure 2. Terminology and measurements of protoconch
used in this paper. The arrow a points to the protoconchteleoconch boundary. The illustrated gastropod has 2' /8
volutions.

Recent and fossil specimens of Cryptonatica species used for comparison of protoconch morphology.
Species

Cryptonatica andoi (Nomura)C. ciausa (Broderip and Sowerby)

C. janthostoma (Deshayes)
C. wakkanaiensis (Habe and Ito)

C. hirasei (Pilsbry)

Locality and age
Mikawaissiki, Aichi Prefecture, central Japan,
RecentOga Peninsula, Akita Pref., northern Japan,
Shibikawa F. (upper Pleistocene)
Toyama Bay, Toyama Pref., central Japan,
RecentMuroran, Utiura Bay, Hokkaido, Recent
Off wakkanai, Hokkaido, Recent
Off Wakkanai, Hokkaido, Recent

No. of specimens andrepository (UMUn
4 (RM 19865 1 ~4)
2 (CM 19866 - 1 ~2)
1 (RM 19867)
5 (RM 19868 - 1 ~5)
7 (RM 19869 - 1 ~7)
4 (RM 19870 -1 ~4)

422

Shin'ichi Nishinosono

After having determined the taxonomic relationships,
faunal characteristics of each sample were analyzed.
Almost all gastropod species identified are extant. The
biogeographic distributions of the species were determinedaccording to the data of living species in the north Pacific(Higo and Goto, 1994). Species living south of N35° are
considered warm-water species and those north of N35° are
cold-water species. Species occurring in both realms weretreated as moderate-water species. These criteria wereused to examine historical changes of the gastropod fauna.
For determination of developmental types in Cryptonatica
from the Oga Pleistocene, protoconch morphology andmorphometry of several species of Cryptonatica from theJapanese coast were examined and compared with fossil
specimens. All the specimens utilized are housed in the
University Museum, University of Tokyo (UMUT).
Furthermore, the type of C. andoi and other specimens
which have been described as C. andoi were examined forcomparison. They are stored in the Institute of Geoscience,
University of Tsukuba (IGUT), Institute of Geology andPaleontology, Tohoku University (IGPS), and Geologicallnstitute, Yokohama National University (GIYU).

Laboratory methods
Observations of the early shell portion of each gastropod
specimen were made with optical and scanning electron
microscopy (SEM) (Hitachi Model S-2400). The protoconch-teleoconch boundary can be recognized easily under
the SEM by the sudden appearance of growth lines.
Protoconch diameter was measured after the removal oflater whorls from the protoconch region exposing theprotoconch-teleoconch boundary (Figure 2). Because
abrasion or dissolution has removed the protoconch surface
in many specimens, whorl volutions of protoconch werecounted at the point that the outer lip and suture line
crossed. Likewise, because of poor preservation, it isdifficult to distinguish the protoconch I (PI)-protoconch II (PII)
boundary in most specimens. For this reason, the shell
diameter at the first half volution (f.v.) was measured andused as a relative size of protoconch I. Measurements weremade by means of a micrometer (accuracy±O.o25 mm)
attached to an optical microscope.
Determination of the mode of development
Developmental types in marine benthic invertebrates including gastropods fall into three main categories; pelagic(planktic) development, direct development, and ovoviviparity(Thorson, 1946, 1950). Pelagic (planktic) development isfurther classified into planktotrophic (larvae) feeding on
phytoplankton during the veliger stage) and lecithotrophic(larvae feeding on egg yolk during a relatively short pelagicstage) (Thorson, 1950). Jablonski and Lutz (1980) summarized and modified Thorson's (1946, 1950) categories, grouping
lecithotrophic, direct, and ovoviviparous development into
non-planktotrophy, so that the modes of development inmolluscs are classified into two major categories, planktotrophy and non-planktotrophy. Their classification is adopted
in this paper.
The modes of development of Pleistocene samples of

Cryptonatica have been examined on the basis of culture
experiments of living species (Table 1) and the morphologicalcharacteristics of the protoconch with species whose earlylife histories have been well documented. The family
Naticidae is known to include both planktotrophy and nonplanktotrophy (Thorson, 1950; Giglioli, 1955; Bandel, 1975 ;Amio, 1955,1963; Appendix 2).

Results
Historical changes in faunal composition
The frequency of warm-water species increases towards
the top of the section, with a gradual decrease in the

Sampling
Horizons

A-7
A-6
A-5
A-4
A-3

A-2
Anden
A-I
Shell Beds

ji

Upper
S-10
S-9
Shell Beds S-8

<

i i i

~;;
i

i

S-7
S-6
S-5
S-4
S-3
S-2

Lower
Shell Beds S-1

o

5

10

N umber of Species•x•Warm water species
Intermediate species
Cold water species

Figure 3. Historical change of gastropod faunal composition in the upper Pleistocene sequence of the Oga Peninsula.

1009. Larval paleoecology of late Pleistocene Cryptonatica
frequency of cold- water species (Figure 3). No majorchange in litho- and biofacies is recognized in the marine
shell beds studied, suggesting that the sediments were
mostly deposited under a similar environmental setting ofshallow shelf to intertidal zone. These lines of evidence
correlate well with the results of molluscan faunal analysis by
Takayasu (1962) and both strongly suggest a gradualincrease in the influence of the warm Tsushima currents
from the south during 100-134 Ka.

Protoconch morphology and variation in Cryptonatica
There are two protoconch morphotypes in the specimens
of Cryptonatica from the upper Pleistocene sequence in the
Oga Peninsula. One morphotype here named S- type, has asmaller protoconch (0.8 to 1.13 mm in diameter) and a larger

423

number of volutions (2 to 2.5) (Figures 4- 1a, b). The othermorphotype here termed L- type, is characterized by a larger
protoconch (0.95 to 1.4 mm in diameter) with a smaller
number of volutions (1.5 to 2) (Figures 4- 2a, b). No intermediate specimen has been found in the material examined(Figure 5). These two morphotypes cannot be distinguishedby other shell features. L- type occurs abundantly in the
Shibikawa Formation and the lower part of the Anden
Formation (A- 1), but is rare in the middle to upper part of the
Anden. In contrast, S- type is rare in the Sibikawa Formation, although it occurs abundantly in the Anden Formation(Figure 6).
Specimens of L- type exhibit remarkable variations in the
diameter and number of volutions of protoconch at eachhorizon. The protoconch diameter of specimens from the

Figure 4. Scanning electron micrographs of the protoconch region of Cryptonatica . 1. A specimen of S- type(0. andoi), UMUT CM 19863- 1, Loc. A- 3, Anden Formation, a : overall view, b : close - up of the apical part marked
by an asterisk in a. 2. A specimen of L - type (C. sp. aft. 0. andoi), UMUT CM 19864- 1, Loc. S- 1, Shibikawa
Formation, a : overall view, b. close- up of the apical portion marked by an asterisk in a. Arrows in 1a and 2b point
to the protoconch- teleoconch boundary. Scale bars : 100 ,u m for 1a, 2a ; 10,um for 1b, 2b.

Shin'ichi Nishinosono

424

L - type

1.5EE.Q)...

Q)

E
co

C
J:
U

y

1.4
1.3

o
o

1.2

1.25 X - 1.86, r = 0.62

•
o

0.9

o

0.8

a..'-

y

1

o(.)

-

S - type

1.1

s:::::o1.75 X - 1.95, r = 0.60

•

;:

2

2.2

• /•

0.7
1.4

1.6

1.8

2.4

2.6

Number of Volutions
Figure 5. Scatter plots of protoconch diameter versus protoconch volutions in the late Pleistocene specimens
of Cryptonatica from the Oga Peninsula. Black circles: S-type (C. andoi), white circles: L-type (C. sp. aff. C.
ando/). Regression lines by least-squares fit.
upper shell beds of the Shibikawa Formation (S-8~S-10) is
generally larger than that of specimens from other horizons(Figure 6). There is a positive linear relationship between
the diameter and the number of volutions in the protoconchof specimens of this type from each horizon (r=0.6) (Figure5). There is, however, little variation in the average diameterof the first volution in L-type specimens from different
horizons. There is no significant variation in protoconch
size or volutions in the S-type specimens.

Inferred mode of development in Cryptonatica
Culture experiments of snails from Hokkaido have shownthat larvae of C. andoi are planktotrophic (Amio, 1955; Table
2). Amio (1955) described a distinct granulation on the
protoconch surface that formed during incubation. Recent
specimens of this species from off the Mikawaisshiki area,
Pacific coast of Central Japan, also have this granulated
ornamentation on the PI surface (Figure 7-2). Four specimens from this area have a relatively small Protoconch I(mean t.v. value=0.12 mm), a larger number of protoconch
volutions (mean value=2.38) and a small protoconch diameter (mean value = 1.20 mm) (Table 2).
The late Pleistocene S-type specimens of Cryptonatica
from the Oga Peninsula are very similar to the specimens of
C. andoi shown by Amio (1955, fig.8) and those from off
Mikawaisshiki (Figures 7-1, 2), in the size, shape, and orna-

ment of protoconch and teleoconch, suggesting a planktotrophic mode of development in the former.
In contrast, the upper Pleistocene Cryptonatica specimensof L-type from the Oga Peninsula are similar in the size andshape of protoconch to those of C. c/ausa, Polinices josephina, and Neverita vesica/is, all of which have non-planktotrophic development (Bandel, 1975; Giglioli, 1955; Amio,
1955). These observations suggest that Cryptonatica of Ltype had a non-planktotrophic development. No distinct
granulated ornamentation is observed on the protoconch
surface of L-type under the SEM (Figures 4-2a, b).
Distinct granulation also occurs on the protoconchs of C.
janthostoma (Figures 7-3, 4) and C. wakkanaiensis (Figures 75, 6), whose size and volution numbers are compared withthose of S-type specimens of Cryptonatica from the Oga
Pleistocene and of extant specimens of C. andoi. In view ofthese morphological data, the former two species may havea planktotrophic development (Table 2).

Discussion
Taxonomic and ecological relationships of L- and S-types
Two protoconch types, L- and S-types, have been distinguished in specimens of Cryptonatica from the upper Pleistocene deposits in the Oga Peninsula. Available data on
the relationships between protoconch morphology and mode

1009.

-

1.- •

A-7 1
A-6 1
A-S 1
A-4

••

A-3 1
A-2 1

A

1

~

t::J

n

S-7 1

~

~

n

=

S-4 1
S-3 1

0.1

•

c:J
c:J

0

l
l
l

~

0

I'-L

1.5

Diameter of first volution (mm)S-type•••-_ ... odo
•

.~

•

•

2.5

1

0.75

Volutions

0

~

!:l

,r'l 1:1

•

=

l
l
l
l
2

425

•

l
l
l

....

=

8rL In ~
t::J

0.25

•

-

l

l
l
l
l

t::J

s-s 1

l
l
l
l
l
l
l

..-••

l

S-9 1
S-8 1

S-l

l
l
l
l
l

c:J

A-I 1

S-10

Larval paleoecology of late Pleistocene Cryptonatica

=

!:l
!:l

Ijjl
-0

•

Q;Cl~
1

1.25

1.5

Protoconch diameter (mm)D L-type

Figure 6. Variation of the number of volutions and size of protoconch in two morphotypes of Cryptonatica inthe upper Pleistocene sequence of the Oga Peninsula. Specimens of L-type (C. sp. aft. C. andoJ) have been
replaced by those of S-type (c. andoi) toward the top of the sequence.

Table 2. Measurements of protoconch and mode of development in six species of Cryptonatica. All specimens
excluding C. clausa are Recent specimens. t.v.: diameter of the first half volution. Number of specimens is shown inparentheses. Measurements are shown by sample means for those species which represented by more than two
specimens. Developmental modes of C. clausa, C. andoi and C. adamsiana were determined by culture experiments andthose of other three species were inferred from comparison of protoconch morphology with naticid species whose
developmental modes are known (see Appendix 2).
SpeciesC. andoi

C. c/ausa
C. janthostoma

C. wakkanaiensis

0.12 (4)0.28 (3)0.14 (5)0.12 (1)

Number of
volutions2.38 (4)1.81 (3)2.39 (3)2.25 (1)protoconch
diam. (mm)1.20 (4)1.38 (3)1.16 (3)0.94 (6)0.26 (4)2.23 (4)1.76 (3)t.v. in mm

C. adamsiana

C. hirasei

of development in extant naticids strongly suggest that thetwo morphotypes probably underwent different modes ofdevelopment; namely planktotrophy for S-type and nonplanktotrophy for L-type. They, however, cannot be distinguished by the teleoconch morphology.
Two interpretations are possible for the taxonomic relationship of these two morphotypes. One is that they represent discontinuous variation in a single biological species

Mode of development
Planktotrophy (Amio, 1955)
Non-planktotrophy (Thorson, 1950)
Planktotrophy (this study)
Planktotrophy (this study)
Planktotrophy (Amio, 1955)
Non-planktotrophy (this study)

with two different modes of development. This kind of
discontinuous variation in which two or more modes ofreproduction exist within a single species was termed
poecilogony (Giard, 1905). If we accept this interpretation,
the stratigraphic occurrences of L- and S-types in the
Pleistocene section of the Oga Peninsula indicate that nonplanktotrophic development was replaced by planktotrophic
development in a single species lineage during a relatively

426

Shin'ichi Nishinosono

short interval between 130-100 Ka.
The other interpretation is that L- and S-types belong to
two different species. If this interpretation is correct, thesimilarity of teleoconch morphology between the two morphotypes must be explained by convergence. In this case,the two morphotypes may represent cryptic species, since
they cannot be distinguished morphologically except for thedifference in protoconch size and shape.
The genus Cryptonatica was established by Dall (1892) for
naticids with a semicircular callus entirely or largely filling theumbilicus and a smooth operculum in association with a few
grooves along its outer shell margin. He designated Natica
c/ausa Broderip and Sowerby, 1892 as the type species.
Majima (1989) recently summarized the systematics andstratigraphic distribution of Cryptonatica from Japan anddescribed five species, C. ichishiana, C. c/ausa, C. janthostoma, C. adamsiana, and C. andoi, among which C. andoi ismost similar in the overall shell features to the two late
Pleistocene morphotypes of Cryptonatica from the Oga
Peninsula. C. andoi ranges from Early Pliocene to Recent
and is characterized by having a relatively shallow sulcus,
commonly narrow umbilical callus, and an operculum sculptured with two marginal grooves on the exterior surface. Of
the five Japanese Cryptonatica species, only C. andoi and C.
adamsiana are known to occur in late Pleistocene age in thenorthwestern Pacific region, and they are easily distinguishedby the differences in the development of callus and umbilicus (see Majima, 1989). C. andoi was established by
Nomura (1935, p. 201, pI. 9, figs. 35a-36b) based on a specimen (holotype) from the Upper Pliocene of Taiwan. My
observation of this specimen (IGPS 52295) reveals that it has
a small protoconch, measuring 2.5 volutions and 0.15 mm in
the diameter of the first half volution, which is similar to theprotoconch of S-type specimens from the Oga Peninsula.
The S-type specimens of late Pleistocene Cryptonatica fromthe Oga Peninsula are, therefore, identified as C. andoi.
Living samples of this species from off Mikawaisshiki,
Central Japan, and Muroran Bay, southern Hokkaido (Amio,
1955), consist of S-type only, and no extant specimens of Ltype have been found in this species around the Japanese
coast.
According to Majima (1989), c. andoi exhibits a relatively
wide but continuous variation in callus development atmaturity, and no discontinuous variation has hitherto beenreported in teleoconchs. Of the specimens described as C.
andoi by Majima (1988), the following four early Pleistocene
speCimens are similar to L-type specimens from the Oga
area: GIYU 531-3 and 4, both from the Sawane Formation,and IGUT 16004-3 and IGUT 16004-3, both from the Omma
Formation.
We have at present no data on the genetics or soft

anatomy which would allow us to determine whether L- andS-types are dimorphs of a single species (c. ando/) or
represent two different species, but current knowledge ofearly life history of extant marine invertebrates may provide
some useful comparisons. Recently it has become clearthat poecilogony is rare in marine invertebrates (Hoaglandand Robertson, 1988; Bouchet, 1989). Many examples of"poecilogony" have been shown to be two reproductively
isolated, cryptiC species. Levin et a/. (1991) demonstrated
that the polychaete Streb/ospio benedicti is a rare case oftrue poecilogony, and that the traits associated with the twodevelopmental modes have a clear genetic basis.
It is not easy to maintain two developmental modes in a
population. Therefore, it appears that shifts in mode of
reproduction usually occur rapidly and completely within
populations, leading to reproductive isolation and hence
speciation (Hoagland and Robertson, 1988; Bouchet, 1989).
Judging from these lines of indirect evidence, it can be
postulated that L- and S-types of Cryptonatica represent
closely allied, but different species, though the ancestraldescendant relationship between them is still uncertain. Ltype is assigned to an undescribed species, but in this paper,
it is provisionally placed under Cryptonatica sp. aff. C. andoi
until an adequate taxonomic survey of large samples is
made.

Summary and conclusions
1. Faunal analysis of gastropod assemblages from theupper Pleistocene marine sequence in the Oga Peninsula,northern Japan, shows that the frequency of warm-water
species increases towards the top of the sequence, with a
gradual decrease in the frequency of cold-water species.
This reflects a gradual increase in the influence of the warm
Tsushima currents from the south during 100-134 Ka.
2. The upper Pleistocene specimens of Cryptonatica fromthe Oga area consist of two morphotypes that can only be
distinguished by the difference in size and shape of the
protoconch. They are comparable in teleoconch morphology to C. andoi. The relationship between protoconchmorphology and mode of development in extant species of
the Naticidae strongly suggests that the two morphotypes
underwent different modes of development; i.e. planktotrophy for the type with a smaller protoconch (S-type) and nonplanktotrophy for the type with a larger protoconch (L-type).
The non-planktotrophic form was replaced by the planktotrophic form in the Oga Pleistocene during a relatively
short interval between 130-100 Ka.
3. The two morphotypes of Cryptonatica can be interpreted as closely allied different species (cryptic species) rather
than dimorphs of a single species with different develop-

Figure 7. Scanning electron micrographs of the protoconch region of the three species of Cryptonatica. Overall apicalviews (1, 3, 5) and close-up of the granulated ornament on the apical portion (2, 4, 6; pointed by short arrows). 1-2. C. andoi.
Two specimens from off Mikawaisshiki, Central Japan. UMUTRM 19865-1, 2. 3-4. C. janthostoma. Two specimens fromoff Muroran, southern Hokkaido. UMUT RM 19868-1,2. 5-6. C. wakkanaiensis. Two specimens from off Wakkanai,
northern Hokkaido. UMUT RM 19869-1,2. Arrows in 1,3, and 5 point to the protoconch-teleoconch boundary. Scalebars: 500,um (1,3,5) and 50,um (2,4,6).

1009. LaNai paleoecology of late Pleistocene Cryptonatica

427,

Shin'ichi Nishinosono

428

mental modes (poecilogony). Comparison with the type andfigured specimens of Cryptonatica indicates that S-type
specimens are identified as C. andoi, whereas those of Ltype belong to a new species, here provisionally described as
C. sp. aft. C. andoi.

Acknowledgments
I thank Prof. Kazushige Tanabe (University of Tokyo) for
his supeNision of this study and for critical reading of the firstdraft, Dr. Ryuichi Majima (yokohama National University) for
providing me with critical comments on taxonomy of
Cryptonatica, and Dr. Tatsuo Oji, Mr. Masaaki Shirai andother colleagues in the Geological Institute of the Universityof Tokyo for their helpful advice both in the field and laboratory. I also acknowledge Dr. Tomoki Kase (National Science Museum) and Mr. Toshiya Miyauchi for critcal review ofthe manuscript and providing me with recent specimens, Dr.
David L. Dettman (University of Arizona, Tucson) for correcting the English, and Dr. R. Majima, Prof. Kei Mori (Tohoku
University), Prof. Kenshiro Ogasawa and Prof. Hiroshi Noda
(University of Tsukuba) for arranging loans of type collectionsin their care.

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Matoba, Y., 1992: Recent advancement in Late Cenozoic
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57, no. 4, p. 319-333. (in Japanese with English abstract)
Matsumoto, T., Uno, K., Ono, K. and Watanabe, K., 1991.
K-Ar age of the Aso Volcanic rocks-Consistency withvolcanostratigraphy and application to pyroclastic flow
samples-. Programs with abstracts of the 1991-1992
meetings of the Volcanological SOCiety of Japan, p.73.
Nagatomo, T., 1990: Geochronology of tephra by TL and
ESR methods. Chikyu Monthly, vol. 12, no. 2, p.74-79.
(in Japanese)
Nomura, S., 1935: Catalogue of the Tertiary and Quaternary
Mollusca from the Island of Taiwan (Formosa) in theInstitute of Geology and Paleontology, Tohoku Imperial
UniverSity, Sendai, Japan. Part 2. Scaphopoda and
Gastropoda. Science Reports of the Tohoku Imperial
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Oba, T., 1991: Aso 4 and Ata Tephra in view of oxygenisotopic stratigraphy. Chikyu Monthly, Vol. 13, no. 4, p.
224-227. (in Japanese)
Okaguchi, M., 1978: Fission track dating of the obsidiansfrom pyroclastic flow deposits. Bulletin of the Volcanological SOCiety of Japan, Series 2, vol. 23, no. 4, p.
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Shirai, M., 1995MS: Paleo-water depth and its relationshipwith sedimentary facies of late Pleistocene shallowmarine sediments at the Anden Coast, Oga. Master
Thesis for the Geological Institute, Graduate School of
Science, University of Tokyo.
Shuto, T., 1974: Larval ecology of prosobranch gastropoda
and its bearing on biogeography and paleontology.
Lethaia, vol. 7, no. 2, p.239-256.
Shuto, T., 1994: Systematics and evolution. In, Habe T.,

1009.

Larval paleoecology of late Pleistocene Cryptonatica

Okutani, T. and Nishiwaki, S. eds., Handbook of
Malacology, vol. 1, p.217-246. Scientist Book Publishing Co., Tokyo. (in Japanese)
Takashima, I., Yamazaki, T., Nakata, E. and Yukawa, K.,
1992: TL age of the Quaternary volcanic rocks andpyroclastic flow deposits around the Lake Toya, Hokkaido, Japan. Journal of Mineralogy, Petrology andEconomic Geology, vol. 87, no. 5, p.197-206.
Takayasu, T., 1962: Molluscan fossils from the Shibikawa
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429

University, Series A, vol. 2, no. 2, p.1-19.
Thorson, G., 1946: Reproduction and larval development ofDanish marine bottom invertebrates with special reference to the planktonic larvae in the Sound ((Z)resund).
Meddelelser fra Kommissionen for Havundersogelser,
Serie Plankton, vol. 4, p.1-523.
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Wary, G.A. and Raft, R.A., 1991 : The evolution of developmental strategy in marine invertebrates. Tree, vol. 6,
no. 2, p. 45-50.

Shin'ichi Nishinosono

430

Appendix 1. List of gastropod species from the upper Pleistocene of the Oga Peninsula.
water species, w: warm-water species, i: intermediate species.

c: cold-

S-3 S-4 S-5 S-6 S-7 S-8 S-9 S-I A-I A-2 A-3 A-4 A-5 A-6 A-7
Snecies2
178 4
2
Notoacmea concinna Lischke
Buccinum so.
I
Siphonalia sp.
I
Cerithiopsidae Notoseila laaueata Gould
4
6
17 22 3 4
Cocculina kurapien.!is Yokoyama)
Cocculinidae
to 3I
Cacculina 'aDonica Dan
I
Eulima ozawai Yokoyama
Eulimidae
2
EmarRinula fraoilis Yokoyama
Fissurellidae
II
2
I 15 19 to 18 3
I 13 I
5Punctrella nobilis A. Adams
4
4
3
6
I
I
EDheria decorata A. Adams
Lacunidae
I
Lamenariidae Velutina conica Dan
I
I
3 II 9 52 3
4
5
Acmaea Niveotectura pallida (Gould
Leoetidae
1
Liotina semiclathratura Schrenck
Liotiidae
I
I
BoreotroDhon candelabrum Reeve
Muricidae
I
PteroDumura adunca SowerbYl
2
Pterooumura adunca Sowerbvl
I
4
2
2
unker
Reticunassa multipranosa
Nassaridae
1
2
2
3
6
2
8
3
Crvntonatica ando; Nomura
Naticidae
I
Crvntonatica c/au.!a Broderin and Sowerby)
1
Eunaticina DaDilla Gmelin
1
6 2
I
Eusnira pila (Pilsbrv)
I
Glossaulax didvma didvma Rodino\
22395 10 155 2 12 I
Olivella fulpurata A. Adams and Reeve
OlividaeI
fPvramidellidae Leucotina e;pantea Dunker
I
Odostamia SP.
1
91
Turbonilla subnlanicostata Yokoyama
Turbonilla SP.
2
I
9
3
3
1 2
Pyrenidae
Mitrella bicincta Gould
I
I
Rhiwrus cvlindrella A. Adams
Retusidae
Rhizorus radiolus A. Adams
2
Rhizorus sn.
16 I 77 39 31 13 44
Rimlicula doliaris Gould
I
1
I
Rin~iculidae
RinRicula sp.
Scaohandridae Cvlichna consabrina Gould
I
1
Trichotropidae Trichamathina nobilis A. Adams
Trillhoridae
Triphora SP.
I
1
Trochidae
Callioslonuz multi/iraturn Sowe~
1
Calliostoma SD. 1
1
Calliostoma so. 2
I
Calliostoma sn. 3
I
Cantharidus "essoensis Schrenck
1
Cantharidus callichroa PhiliDDi
3
Cantharidus sn.
2
Lirularia Dvpmaea Yokoyama
12 11
Lirularia so.
25Minolia Dunctata A. Adams
522
Marmrites laudatus Yokoyama
2
I
2
I
2
Trochidae so. I
8Trochidae so. 2
1
Trochidae so. 3
1
I
Turbinidae
Homalonoma amussiatum Gould
7245
2 13 15 198 39 22 6
1 3 14
HamaloDoma so.
2
Turridae
Etremooa subauri ormis E.A.Smith
1
I
I
C athrodrillia sn.
Manpelia semicarinata (Pils~
1
Manl!elia tabatensis Tokuna.a12Manpelia sn.
2
1
I
OenoDota okudai Habe
I
Ophiodermella mivatensis Yokoyama
2
ODhiodermella psedopannus Yokoyama
4I
91
Ophiadermella SD.
Propebella vokovamai Onovama
25 7 15 10 10 2121
5Prollebella so.
1
Pseudaetrema onilirata (E. A. Smith
13I
Turritomella candida Yokovama
12Turridae so. 1
2
2
Turridae so. 2
I
Turridae so. 3
2
Turridae 50.4
Turridae sn. 5
II
Turridae 50.6
1
1I
Turridae 50.7
8
Neohaustator andenensis Otuka
Turritellidae
412Turritella otukoi Kotaka
31ITurritellidae. 2en. et so. inde!. I
Turritellidae.•en. et sn. indet. 2
35 22 81 14 21 53 112 267 536 61 129 60 47 31 72
Number of snecimens
7
5
3
2
3
2
7
7
6
5
1 5 3
9
Number of cold-water s"".ojes
7
4
4
4
4
7
7
6
5
5
3
1 3
1 0
Number of intermediate SPecies
1
3
1
3
0
0
0
3
I
I
I
1
I 0
Number of wann-water s~cies
1 0
FamilvAcmaeidae
Buccinidae

i

?
?
i

?
c
w
w
c
c

?
c
w
i
i
i
i
i
c
w
c

?
i
w

?
w

?
i
c
i

?
i

?
c
c

?
w

?
?
?
c
w

?
c

?
w

?
?
?
?
c

?
i

"'!
w
w

?
c
i
w

?
c

?
i
c

?
?
?
?
?
?
?
c

?
?
?

1589

1009.

LaNai paleoecology of late Pleistocene Cryptonatica

431

Appendix 2. Mode of development and measurements of protoconch in 14 species of the Naticidae. t.v.:
diameter of the first half volution, Pt: planktotrophic, P: planktic either planktotrophic or lecithotrophic, D: direct
development. Species with a small f.v. value «0.21) indicate planktotrophic or at least planktic. P. sagamiensis is thought to have a lecithotrophic laNai stage in view of its relatively short planktic period.
Species

AuthorPolinices hepaticus
P. /actes
P. triseriata
P. sagamiensis
P. josephina
P. herosP. duplicata
Natica pal/ida
N. canrena
N. macu/osa
Neverita vesica/is
N. rainiata
N. didyma
Sinum papilla

Bandel, 1975
Bandel, 1975
Giglioli, 1955
Amio, 1963
Giglioli, 1955
Giglioli, 1955
Giglioli, 1955
Thorson, 1950
Bandel, 1975
Amio, 1955
Amio, 1955
Amio, 1955
Amio, 1955
Amio, 1955

Hatching shellsize (mm)
0.28
0.40
0.52
0.46-0.64
0.78
0.13-0.15

Diameter oft.v. (mm)
0.10
0.10
0.16
0.21
0.20
0.093

Development
type
Pt
Pt
P
P
D
P

1.7
0.56
0.26-0.28
1.0
0.32
0.45
0.16-0.22

0.31
0.17
0.11
0.31
0.13
0.17
0.09

D
Pt
P
D
P
P
P

ru8

ruo

P

Pelagic period
Unknown
Unknown
Unknown
2 weeks
Unknown
Unknown
Unknown
3-4 weeks
3 weeks
3 weeks
3-4 weeksTrans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.432-447, 14 Figs., June 30, 1996
© by The Palaeontological Society of Japan 1996

The first reliable record of Beremendia (Insectivora,
Mammalia) in East Asia and a revision of Peisorex
Kowalski and Li, 1963
CHANG-ZHU JIN AND YOSHINARI KAWAMURA
Institute of Vertebrate Paleontology and Paleoanthropology, Academia Sinica, P.o. Box 643, Beijing, China
Department of Earth Sciences, Aichi University of Education, Kariya, Aichi Prefecture, 448 Japan

Received 17 November 1995; Revised manuscript accepted 22 February 1996
Abstract. Well preserved large shrew remains with pigmented teeth were recovered from early Pleistocene fissure sediments at Haimao, Dalian, northeast China. They are assigned to the genus Beremendia on the basis of their morphological characters. The monospecific genus Peisorex previously described from the early Pleistocene of north China is synonymized with Beremendia, because no basic
morphological differences indicative of generic distinction exist between them, and its sole species, P.
pohaiensis, therefore becomes Beremendia. Comparison with the holotype of this species reveals thatthe remains from Haimao belong to Beremendia pohaiensis. Moreover, it is newly recognized that
"Peisorex p/iocaenicus" recently described from the middle Pliocene of north China is conspecific with B.
pohaiensis.
The remains from Haimao provide us with much knowledge on the morphological characters of B.
pohaiensis, which is distinct from other known species of Beremendia. The occurrence of B. pohaiensis
is the first reliable record of the genus in East Asia, because previous records of Beremendia from East
Asia lack sufficient grounds in identification. Beremendia has been known mainly from the early Pliocene
to middle Pleistocene of Europe. B. pohaiensis indicates that Beremendia was distributed both in Europe
and East Asia from the middle Pliocene to early Pleistocene. This genus had probably migrated from
Europe to East Asia by the middle Pliocene.
Key words: Beremendia, Peisorex, early Pleistocene, northeast China, systematics, paleobiogeography

Introduction
Beremendia, a large extinct shrew with pigmented teeth,
was first established by Kormos (1934) on the basis of
specimens from Villany, south Hungary. It has been recorded from a number of Pliocene to middle Pleistocene fossil
localities in Europe, but is unknown in East Asia except forthree questionable records from north China, which are too
insufficient to prove its distribution greatly remote from
Europe.
In June 1989, fossiliferous fissure sediments were found ina limestone quarry at Haimao (Figure 1). The sediments
were preserved in two small pockets at different altitudes(Sun et al., 1992). The excavations conducted in 1989 and1990 revealed that the sediments of the lower pocket yielded
abundant micro-mammalian remains of early Pleistocene
age, including well preserved large shrew remains withpigmented teeth. The morphological characters of theremains indicate that they are assignable to the genus
Beremendia. This occurrence is, therefore, the first reliable

record of the genus in East Asia.
Previously, Kowalski and Li (1963) described a new genus
and species of large shrew from early Pleistocene cavesediments at Chiachiashan about 300 km west-north-westof Haimao, based on a single mandible with pigmented
molars. They designated the mandible as the holotype of a
new species, Peisorex pohaiensis. Since that time, theholotype has been the only specimen referred to the species.
We compared the holotype with mandibles of Beremendia
from Haimao, and found that there were no basic morphological differences between them. Thus, we consider
that Peisorex pohaiensis is conspecific with Beremendia
from Haimao. In this paper, we provide a revised genericdiagnosis of Beremendia which includes Peisorex as asynonym, and describe the remains of Beremendia from
Haimao in detail. On the basis of the description, we
discuss the systematic position and paleobiogeographic
significance of the remains, as well as the taxonomic problems of Peisorex.

1010.

First reliable record of Beremendia

433

BOHAI SEAYELLOW SEA

Figure 1. Location of Haimao in Dalian, northeast China.

Geological setting

The quarry is excavated on the southern slope of Beishan(meaning "north hill") at Haimao, near the coast of DalianBay. According to Sun et a/. (1992), the fossiliferous sediments had originally filled a fissure, about 40 to 50 m long inan east-west direction, which formed in Precambrian limestone. Most of the fissure had been already destroyed bylimestone quarrying to leave the two pockets of different
altitudes before the first excavation began. Yellow clay
about 1.5 m thick infilled the upper pocket, the base of which
is located about 60.5 m above sea level. Mammalianremains and the 14C age on fossil bone indicate that the clay
is late Pleistocene in age. The lower pocket was filled withreddish brown mud of about 0.5 m in thickness. The bottomof the pocket is about 59 m above sea level. This mud
yields 28 forms of micro-mammals including the specimens
described herein, and is considered to be of early Pleistocene age on the basis of its faunal characteristics (Sun eta/., 1992; Xu and Jin, 1992).
Terminology and measuring method

The terminology and measuring method used here are
given in Figure 2. The terminology mostly follows that of
Reumer (1984) with slight modifications. In the figure, we
also add terms generally used for the skull and those usedin Kawamura (1992) for the molars (pre-ectoflexus and postectoflexus). The following measurements have been taken
for the skull and upper tooth row (A and B in Figure 2) :LPL: length from the anterior tip of the premaxilla to theposterior margin of the lacrimal foramen

WR: maximum width of the rostrum measured at N
WUI: width across the first upper incisors
U-N: length from the first upper incisor to N
U-Ml: length from the first upper incisor to Ml
Measurement of the mandibles follows that of Reumer(1984) in order to allow comparison with his abundant data.
The following parameters are adopted (D and E in Figure 2) :LMH: length from the mental foramen to the uppermost
point of the lower margin of the ascending ramus
HC: height of the coronoid process
LUF: length of the upper facet
As regards the lower tooth rows, the following parameter is
exclusively measured (C in Figure 2) :LP4-M 2 : length from P4 to M2
Measurement of the teeth except Nand P4 also follows
that of Reumer (1984) for the same reason. The following
parameters are measured (D and F-I in Figure 2):
AW: anterior width
BL: buccal length
H: height of the first upper incisor
L: length
LL: lingual length
LT: length of the talon
PE: length to the posterior emargination
PW: posterior width
TAW: talonid width
TRW: trigonid width
W: width
Among these, BL, LL and PE of Ml and M2 are used for
calculating the PE-index by the formula, {(LL + BL)/2PE} -1.
This index was introduced by Reumer (1984) to quantify the
degree of posterior emargination of these teeth, which isChang-zhu Jin and Yoshinari Kawamura

434
anterior palatal foramenAB

ros~rum~ :--LPL---l
L.. first upper incisor

ccoronoid processinternal temporal fossa
Dupper sigmoid notch, / pterygoid spicule "~ upper pterygoid fossa ' "first lower incisor

E

.p",

.~irst lower

upper facet
interarticular area\,.,Q~b="=:::~kt;;.J-/ ,nc,sor

condyle {'lower facet 1--e.-O.o,-mandibular foramen
postero-lingual basin of PlosymphysisF. ..parastyleG:, - ' - L - i,bl--:--------,

IH
bi. ' pre-ectoflexU5

'

I

....

....

~esostyleI metaconid-A;.
trigonid basin.,.

'd crest
r·entocon~; ;entoconid\

bl-I--f'-~ ~,t,~pa;~~;~~~~:::-l~:.~:/ ~7';:'>":~!1~~::~~~~~~~~:Spara::~~!~~\ ~U. J/:"7~1~~nid

:..,

.

H

I

~,'root! .:t~:i~~------..t.
:-LT-:!

I :. .

__ .poste~ior.

I \:. .T

"

-

,""

poster~or
emarginationbasin'- ~ ;\.~"'r\0 :TAW,emarg,nat>an .,' •...'.. 1
I : ..... \ ",;,..1h.dIt·· ypoconl'~'''''::~1i=--: :... ·~·-:::L·-- ~ ~~-_·~~talonbasinprotoconid ...i_··_ _ L~r- W : ?to...

<'--.. 'protocone .. ··1--LL---:hypocone

AW:

"""PW

trigon bas·in./ :-PE--::·· .. :protocone'":--LL~;"'hypOcone

TRW: '\.V---1;---

I""'hypoflexid

Figure 2. Terminology and measuring method (based mainly on Reumer, 1984). A: ventral view of the skull,
B: lateral view of the skull, C: lingual view of the mandible, D: buccal view of the mandible, E: posterior view ofthe mandibular ascending ramus, F: first upper incisor (labial view), G: p4 (occlusal view), H: M' (occlusal view),
I: M, (occlusal view). bl: base line for measurement; see text for other abbreviations.

often regarded as an important character in soricid classification.
On the other hand, the length (L) and width rNI of Nand
P4 are measured in accordance with Kawamura (1993),
where each tooth is fixed, with its main cusps being vertical.
The measurements of the Haimao specimens were takenwith a measurescope (Nikon: MM-11) with an electric digitalcounter (Nikon: CM-65), and the holotypes of Peisorex
pohaiensis and P. pliocaenicus were remeasured with amicroscope (Wild: TYP 308700 HEERBRUGG).
Systematic paleontology
Order Insectivora Bowdich, 1821
Family Soricidae Gray, 1821
Subfamily Soricinae Fischer von
Waldheim, 1817
Tribe Beremendiini Reumer, 1984
Genus Beremendia Kormos, 1934

Type species.-Beremendia fissidens (Petenyi, 1864),
which was originally named Crossopus fissidens.
Diagnosis.-Repenning (1967) and Reumer (1984) de-

scribed the diagnostic characters of the genus. Adding ourobservations to them, we provide the following diagnosis:
Dental formula 1-4-3/1-2-3 or 1-5-3/1-2-3; teeth stained
red to almost black; first upper incisor markedly bifid;
upper antemolars reducing in size from Al to A\ A4 reducedor lacking, and invisible from the buccal side of the skull ;posterior emargination in P' and upper molars moderate;parastyle of M' normal and not strongly developed; coronoid
process leaning anteriorly to varying degree; upper pterygoid fossa markedly or slightly depressed; upper facet
narrowly elliptic to oval; interarticular area very broad, andhaving lingual emargination; lower facet placed greatly
anteriorly, and thus invisible in buccal view; internal temporal fossa deeply pocketed; first lower incisor without cusplets on its cutting edge; its apex markedly bent upward; P4
having two cusps and posterolingual basin; entoconid crestwith various degree of development present in lower molars.
Included species.-B. fissidens (Petenyi, 1864), B. minor
Rzebik-Kowalska, 1976, and B. pohaiensis (Kowalski and Li,
1963). Besides these, B. ucrainica (PidopliCko, 1956) was
described from several Ukrainian localities, but as alreadypointed out by Kowalski (1958, 1960), Sulimski (1959) andRzebik-Kowalska (1976), this species seems to be con-

1010.

First reliable record of Beremendia

specific with B. fissidens .
.Geographic . and geologic distribution.-Europe (Early
Pliocene to middle Pleistocene), west Siberia (early Pleistocene), and north China (middle Pliocene to early Pleistocene).
Discussion.- The holotype of Peisorex pohaiensis (V2671)
stored in the Institute of Vertebrate Paleontology andPaleoanthropology, Academia Sinica, has the mandibular
ascending ramus and lower molars which are very similar to
those of Beremendia fissidens, the type species of thegenus, both in morphology and size. We compare theholotype with plastic casts of B. fissidens from Austria (Nos.
77/212 and 77/215; collection of the same institute), andthe descriptions and illustrations of the same species byHeller (1930), Kormos (1934), Kowalski (1958), Sulimski (1959),
Dehm (1962), Repenning (1967), Rzebik-Kowalska (1972,1976), Meulen (1973), Fejfar and Horacek (1983), and Reumer(1984).
The holotype of P. pohaiensis and B. fissidens share thefollowing features: coronoid process relatively short andnarrow; upper pterygoid fossa clearly depressed; upper
facet narrowly elliptic or oval; interarticular area very broad,and having lingual emargination; lower facet placed very
anteriorly; internal temporal fossa deeply pocketed; lower
molars strongly pigmented and having entoconid crests withthe same degree of development.
Additionally, mandibles of B. fissidens have wide ranges ofmorphological variation in such features as the developmentof the coronoid spicule (absent or inconspicuous in some but
marked in others), anterior lean of the coronoid process (veryweak to remarkable), size of the mandibular foramen (small
to very large), and morphology of the lower part of thecondyle (small to large; its apical part narrow and pointed tobroad and blunt). In the holotype, the coronoid spicule isinconspicuous, the anterior lean of the coronoid process isslight, the mandibular foramen is very large, and the lower
part of the condyle is large and has a broad tip (see A to C
in Figure 10). All of these features fall within the variation of
B. fissidens.
On the other hand, the morphology of the mental foramen
is somewhat different between the holotype and B. fissidens.
In the holotype, the foramen is more anteriorly positioned andlarger. Such a difference is, however, not so decisive as toconsider that the holotype is generically distinct from B.
fissidens, because the foramen of B. fissidens is considerably variable in position (but not so anteriorly as in theholotype), and sometimes opens in a large depression below

M,.
It can be concluded that no striking differences indicativeof generic distinction are present between the holotype andB. fissidens. Thus, Peisorex pohaiensis and B. fissidens
belong to a single genus, although some minor differences,which are specific, are found from observations on the wellpreserved specimens from Haimao described below. The
generic name Peisorex (1963) is antedated by Beremendia(1934), and thus synonymized with the latter.

435

Beremendia pohaiensis(Kowalski and Li, 1963)
Figures 3-12
Peisorex pohaiensis Kowalski and U, 1963, p. 138, fig. 1.
Beremendia sp. Sun et al., 1992, p.34, pi. 1, fig.4a-4d.
Beremendia dalianensis Xu and Jin, 1992, p. 1376 (nomen nudum).
Peisorex pliocaenicus Flynn and Wu, 1994, p. 74, fig. 1, pi. 1, fig. 3.

Emended diagnosis.-Size as large as B. fissidens, butmarkedly larger than B. minor, N lacking, so that upper
antemolars except for p 4 reduced to three in number'mandibular foramen always large and deep, and widel;
connected with internal temporal fossa; buccal cingula oflower molars remarkably undulated and generally narrower
than those of B. fissidens.
Referred specimens.-A fragmentary skull with a left firstupper incisor and left N to M2, and with a right first upper
incisor and right N (DH8950); a left maxilla with p4, M' andM2 (DH8952); a right maxilla with p., M' and M2 (DH8953); aright maxilla with M' and M2 (DH8954); two left first upper
incisors (DH8958, 8959); a fragmentary right first upper
incisor (DH8960); a fragment of right M2 (DH8961); a left
mandible with a first lower incisor, M, and M2 (DH8955); aleft mandibular fragment (DH8956); a right mandible with afirst lower incisor and P4 to M2 (DH8951); a right mandiblewith M, to M3 (DH8957); a fragment of right M, (DH8962).
Storage.-AII the specimens are tentatively stored in the
Dalian Natural History Museum (DH: prefix for provisional
specimen numbers of this museum), but will be transferred to
the Institute of Vertebrate Paleontology and Paleoanthropology, Academia Sinica.
Description. Skull: The external naris is a large opening with a trapezoidal shape in dorsal view. The posterior margin of thenaris slightly protrudes to the front at its medial part, and issituated above N. The rostrum is relatively broad and stout.
An elliptical depression with an oblique axis is observed on
the lateral wall of the rostrum above A'. The infraorbital
foramen opens above the parastyle of M'. It forms a broad
depression which diverges toward the front and reaches
above the parastyle of P4. The lacrimal foramen with around outline opens just behind the infraorbital foramen,
above the anterior part of M'. An oval depression is present
between the lacrimal foramen and the alveolar margin of M'.
The zygomatic process is broad but indistinct. The anterior
palatal foramina are situated between left and right A's, andopen very closely to each other in a single shallow depression. The medial part of the bony palate is relatively
flattened, and from this level, its lateral parts rise slightly toform the alveoli of the upper teeth. The alveoli of A' and N
are present between the first upper incisor and N, whereas
no alveolus is observed between Nand p4, indicating acomplete absence of A4 (Figure 38). The posterior palatal
foramen is placed medial to the middle of M'.
First upper incisor: The cusp is distinctly bifid, namely
having a supplementary cusplet on the medial face (Figure5). The apical part of the cusp including the cusplet isstained red to almost black. The talon is not pigmented. It

Chang- zhu Jin and Yoshinari Kawamura

436

A

o

5mm

Figure 3. Fragmentary skull with incomplete upper dentition of Beremendia pohaiensis from Haimao (DH8950).
A: dorsal view, B : palatal view (anterior part of left N damaged).

is broad mesiodistally, and is trapezoidal to squarish in shapein lateral view, which seems to correspond to the "spadeshaped" morphotype of Rzebik- Kowalska (1976). The lateral root- crown junction line is nearly perpendicular to thebase line of the tooth (bl in Figure 2F), or slightly inclines tothe front. This junction line is straight (in DH8958), or slightly
undulated (in DH8950; Figure 4). An indistinct cingulum isobserved along the junction line. The root is robust, with alongitudinal deep groove on the lower part of the lateral face.
The posterior part of the root is remarkably bent ventrally.

1010.

First reliable record of Beremendia

o

437

5mm
!

Figure 4. Fragmentary skull with incomplete dentition of Beremendia pohaiensis from Haimao (DH8950).
lateral view.

A3 : This tooth is unicuspid, with a rounded triangularoutline in occlusal view. The cusp is biased anteriorly, andthe red pigmentation of its apical part is much lighter than inother teeth. From the cusp, a short ridge runs to the anterior
tip of the crown, and another ridge extends to the posterior
margin of the crown. The posterior part of the latter ridge
rises slightly, possibly representing a vestige of a cusp.
These ridges form a straight line which is oblique to themedian line of the skull in occlusal view. The basal part ofthe crown is surrounded by a cingulum, which is thickest in
the posterobuccal part where the crown protrudes dorsally.
pi: The occlusal outline is a rounded triangle, which isbroader than the "tongue-shaped" type illustrated by
Rzebik-Kowalska (1976, fig. 4). The parastyle is a highconical cusp at the anterior tip of the crown, and its apicalpart is stained red. A weak cingulum surrounds the parastyle. A ridge with weak pigmentation (in DH8950) orwithout pigmentation (in DH8952 and 8953) extends from theparastyle to the anterior face of the paracone. The paracone, the highest cusp, is placed somewhat anterior to the
middle of the buccal part of the crown. It is stained red todark red. A high sharp ridge with strong red pigmentation
runs from the paracone to the posterobuccal corner of thecrown. The lingual part of the crown including theprotocone and hypocone is very low and never pigmented.
The protocone is a small indistinct cusp, which is placed on
the anterolingual margin of the crown near the lingual baseLeftof the parastyle. A small supplementary cusp adjoins theposterolingual side of the protocone. An indistinct valley
separates these two cusps from the hypocone which ismuch higher than those cusps. A low blunt ridge extends
from the hypocone to the posterolingual corner of the crown,
where it is slightly elevated. The posterior margin of thecrown is moderately emarginated (in DH8950 and 8952) orstrongly emarginated (in DH8953).
M': The occlusal outline is roughly a square with rounded
corners. The W-shaped ectoloph is a high sharp ridge, andis strongly stained red to dark red. The parastyle is poorly
developed as in many soricid genera including Sorex, andmuch weaker than in Amb/ycoptus and Anourosorex. The
paracone is situated very near the anterior margin of thecrown. The metacone is the highest cusp of the crown.
The metastyle is a ridge-like elongate cusp, which protrudes
posterobuccally beyond the level of the parastyle andmesostyle, so that the post-ectoflexus is much larger thanthe pre-ectoflexus. No cingulum is observed on the buccal
face of the crown. The lingual part of the crown except forthe protocone shows no pigmentation. The protocone is adistinct cusp with red pigmentation, but it is much lower thanthe ectoloph. From the protocone, a low ridge extends
along the anterior margin of the crown to the lingual base of
the paracone, and another ridge extends posteriorly. The
latter ridge becomes indistinct or extinguished at the central
part of the crown. A shallow broad valley separates thisChang- zhu Jin and Yoshinari Kawamura

438

Figure 5.

Left first upper incisor of Beremendia pohaienA : medial view, B : dorsal view.

sis from Haimao (DH8959).

ridge from the hypocone which is situated at the middle ofthe lingual margin of the crown . The hypocone is much
lower and less developed than the protocone. A low ridge
runs from the hypocone to the posterolingual corner of thecrown. This corner protrudes greatly posteriorly, so that thetalon basin is much larger than the trigon basin. The
posterior emargination is moderate (PE- index : 0.23- 0.27).
M2: The basic construction, pigmented area and thedegree of pigmentation on the crown are the same as thosein M I, but the following features differ from those of MI. The
parastyle is better developed than in M I, and protrudes
buccally beyond the level of the metastyle, whereas themetastyle is much less developed than in MI. The posterior
protrusion of the posterolingual corner of the crown is
weaker than in M\ and the posterior emargination is moderate but somewhat less than in MI (PE- index : 0.18- 0.22).
Mandible : The horizontal ramus is stoutly built relative tothat of Sorex, and attains its maximum height at the posteriorroot of MI. The mental foramen opens below the hypoflexidof MI. The symphysis comprises a pair of ridges elongatedanteroposteriorly and a broad groove between them. It
terminates below the posterior root of MI. The ascending
ramus is broad anteroposteriorly, and leans markedly toward
the buccal side (Figure 7). The coronoid process is narrowand short relative to those of Sorex, Petenyia and Blarinella .
This process leans forward in lateral view. The tip of theprocess is rounded and thickened. The coronoid spiculeand external temporal fossa are inconspicuous (in DH8951
and 8956) or absent (in DH8957). The upper sigmoid notchis high in position, and is not emarginated ventrally, so thatits posterior part is nearly horizontal or slightly sloping
backward in lateral view. The pterygoid spicule forms asmall boss in DH8956 and 8957, but is inconspicuous in
DH8951 (Figures 10 and 11). The upper pterygoid fossa is arelatively large depression with a circular outline on thedorsolingual face of the condyle. The upper facet is transversely narrowly elliptic. Its long axis is set obliquely to thatof the mandible in dorsal view (Figure 11). The interarticulararea is very broad and diverges toward the lower facet(Figures 7 and 12). Its lingual margin is emarginated, whereas its buccal margin is almost straight (Figure 12). The lower
part of the condyle with the lower facet on its ventral side isshifted farther forward and strongly protrudes linguoventrally(Figures 6B, 7, 10 and 11). Its anterior margin is placed on
the same straight line as the posterior margin of the internal
temporal fossa in lingual view. Owing to its anterior position, the lower facet is invisible in buccal view (Figures 6A
and 9). The posterior margin of the lower facet is strongly
emarginated in ventral view (Figure 12). The internal temporal fossa is a very large, deep depression with a triangularoutline in DH8957 (Figure 10). In DH8951 and 8956, however, it is divided into a very deep oval depression in its lower
part and a relatively shallow oval depression in its upper part.
The latter is continuous to a depression just below the tip ofthe coronoid process in DH8951 (Figure 6B). The mandibular foramen is very large and broadly elliptic. This
foramen continues to the internal temporal fossa inside thebony bridge which separates them superficially. The lower
sigmoid notch is not greatly emarginated, and forms a nearlystraight line extending diagonally from the upper facet to thebase of the angular process in lateral view. The lower
pterygoid fossa is represented by a shallow horizontal
groove, which runs from the mandibular foramen to the baseof the angular process. It is accompanied by a ridge along
its lower side. This ridge is continuous to the central ridgeof the angular process. The area below these ridges isremarkably excavated.
First lower incisor: This tooth extends straight forward in
dorsal view (Figure 8). The apical part with red to almost
black pigmentation is strongly bent upward (Figure 6). The
cutting edge is smoothed with no cusplets, which corresponds to the "acuspulate" condition of Reumer (1984, fig. 3).
No cingulum is present along the posterior margin of thecrown. On the lingual face of the crown, a narrow but
marked groove runs from the tip to the root- crown junction.
Another indistinct short groove is observed below the posterior part of the marked groove. The crown reaches below
the posterior margin of P4 on the buccal face.
p" : The occlusal outline is roughly triangular. Two main
cusps are present on the crown. The anterior one is higher,
and biased lingually in occlusal view (Figure 8) The two
cusps are connected by a high sharp ridge which encloses
a posterolingual basin on its lingual side. This basin isshallow and drains steeply posterolingually. The cusps andridge are stained red to dark red. A very thick cingulum isobserved on the buccal base of the crown, where the crownhangs over the root. This overhang is weaker than in
Blarinoides. Another Cingulum on the lingual base of thecrown is also well developed, and ascends along the posterior margin of the crown to form a small cusplet on themargin.
MI and M2 : The occlusal outline is trapezoidal. The
ectolophid with W- shaped occlusal pattern is stained red todark red. Of the ridges forming the ectolophid, a ridgeconnecting the protoconid with the paraconid is much longer
than that connecting the protoconid with the metaconid.
Each ridge has a notch at its middle part. The protoconidis the highest cusp of the crown, and situated anterobuccal

1010. First reliable record of Beremendia

439

A

o

5mm
!

B

Figure 6. Right mandible with first lower incisor, P4, Mr and M2 of Beremendia pohaiensis from Haimao(DH8951). A: buccal view, B : lingual view.

to the metaconid. The hypoflexid steeply descends buccalIy and reaches the buccal cingulum. A ridge extending
anterolingually from the hypoconid descends toward theprotoconid, and attaches to its posterior face. Anotherridge extends lingually from the hypoconid, and forms an
indistinct cusplet at its lingual end. This ridge is separated
from the entoconid by a marked valley. Differing from theother main cusps, the entoconid is a conical isolated cusp
without pigmentation. The entoconid crest connecting theanterior base of the entoconid with the posterior base of themetaconid is low and short in Mr (Figures 68 and 8). In M2 ,however, it is somewhat higher and longer. The trigonidbasin is larger than the talonid basin. The cingulum surrounding the base of the crown is well developed, but muchthinner than that of P4' It is remarkably undulated on the

buccal face (Figure 6A).
M3: The occlusal outline is roughly semicircular. The
trigonid is basically similar to those of Ml and M2 in morphology, but is smaller. On the other hand, the talonid isstrongly reduced, so that the talonid basin is much smallerand shallower than the trigonid basin. A ridge extends
backward from the posterior face of the protoconid, and thencurves lingually to form a small cusp at its lingual end (Figure
8A). This cusp adjoins the entoconid, which is also small
and feeble. The entoconid crest is lacking, so that thetalonid basin opens lingually between the entoconid andmetaconid. The cingulum on the buccal base of the crown
is well developed, while that on the lingual base is weaker,
and interrupted below the metaconid.
Measurement.-The measurements of the skull, mandibles

Chang- zhu Jin and Yoshinari Kawamura

440

o

2mm
!

!

Figure 7.

Posterior view of the right mandible of Bere-mendia pohaiensis from Haimao (DH8951).

Table 1. Measurements (in mm) of the skull and upper
dentition of Beremendia pohaiensis from Haimao.
Element

Para mete r

DH8950

LPL
WUI

7. 28
3.74
3.40

LI-A3
LI - M I

5.27
9. 62

Left firstLupper incisor

H

2. 78
2. 51
I. 28

Skull

WR

Upper tooth

row

LT

Right firstupper incisor

L
H
LT

DH8952

DH8953

DH89543.423.53
2.382.4 1
I. 53
I . 52

2. 70
2. 57
I. 28
O. 94

Right A3

L
W

p4

OL

LL
PE
W
MI

OL
LL

PE
AW
PW

M2

BL
LL
PE
AW
PW

DH 8958 DH8959

1. 23
O. 91
2.5 1 2.7 1
2. 67
2.032. 191. 98
1. 91
1.951.72
2.4 2
2.48
2.4 1
2. 45
2.35
1.95
2.53
2.57

2. 59
2. 50
2. 56
2.39
2. 071.9 5
2. 53
2.57
2.6 1 2. 46

2. 52
2.43
1.94
2.57
2.55

1. 81
1. 80
I. 51
2. 49
1.93

2.0 11.82
1.81
1. 83
I. 57
1.53
2.46
2.4 1
1.90
2.0 1

1.93
1. 80
1.58
2.42
1. 89

Figure 8. Right lower dentition of Beremendia pohaiensis from Haimao. Occlusal view. A: M I - M3 (DH8957), B:
first lower incisor, P" M, and M2 (DH8951).

and dentition are given in Tables 1 and 2.
Systematic position and comparison.- The specimens
undoubtedly belong to the subfamily Soricinae, because theinternal temporal fossa is deeply pocketed, the interarticulararea of the mandibular condyle is emarginated lingually, andP, has a posterolingual basin. On the basis of the key given
by Reumer (1984), characters such as the presence of theentoconid crest, very broad interarticular area of the condyle,strong anterior shift of the lower facet and fissident firstupper incisor indicate that the speCimens are referable to thetribe Beremendiini which comprises a single genus, Beremendia. In addition to these characters, we can observe
the following characters in the present specimens, which are
diagnostic of Beremendia: teeth pigmented; posterior
emargination of p.I and upper molars moderate ; coronoid
process leaning anteriorly; upper pterygoid fossa distinct ;upper articular facet narrowly elliptical; first lower incisor
acuspulate and with the apical part strongly bent upward.
Thus, the specirnens are safely allocated to Beremendia.

1010.

First reliable record of Beremendia

Table 2. Measurements (in mm) of the mandibles and lower dentition of Beremendia pohaiensis from Haimao.
Element

Parameter

DH895 I

DH8956

DH8957

DH8955

LMH
He
LUF

1.18
6.46
I. 86

Lower toothrow

LP, -M2

5.80

First lower
incisor

L

6. 69

P,

L
W

I. 85
I. 45

MI

L
TRW
TAW

2.11
I. 61
I. 69

2.82
I. 46
I. 54

2.76
I. 50
I. 63

M2

L
TRW
TAW

2.34
I. 42
I. 41

2. 34
I. 40
I. 31

2. 15
I. 33
I. 21

M3

L
TRW

Mandible

6.05 ±
I. 59

5. 93
I. 69

Table 3. Remeasurements (in mm) of theholotypes of "Peisorex pohaiensis" (V2671) and "P.
pliocaenicus" (V8900).

We first compare the present specimens with the holotypeof "Peisorex pohaiensis" here called Beremendia pohaiensis.
The holotype is very similar to the present specimens in themorphology of the ascending ramus (Figures 9-12), and there
are no basic differences between them, although the mandibular bone of the holotype is somewhat larger and stouter
than those of the present specimens. The lower molars of
the holotype are also very similar to those of the present
specimens both in morphology and size (Tables 2 and 3).
The present specimens are, therefore, identifiable with
Beremendia pohaiensis.

We secondly compare the present specimens with the
holotype of "Peisorex pliocaenicus" (V8900 stored in the
Vertebrate Paleontology and Paleoanthropology, Academia
Sinica) which was recently described from the middle

P. pO/lOiellsis(V2671)

P. pJiocaellicus(V8900)

L
TRW
TAW

2. 75
I. 10
I. 81

2.11
I. 46
I. 57

M2

L
TRW
TAW

2. 45
I. 54
I. 30

2.21
I. 54
I. 33

M3

L
TRW

I. 10
O. 97

1.65
O. 99

ElemenlParameter

MI

6. 19

I. 58
O. 90

441

Pliocene in the Yushe Basin by Flynn and Wu (1994). The
holotype, the only specimen of the species, is a rightmandible with M I , M2 and M 3 • The morphological characters of the holotype are well coincident with those of thepresent specimens, namely, the position of the mental foramen, shape of the condyle and upper pterygoid fossa,
position of the lower facet, size of each mandibular anddental element (Tables 2 and 3), and other minor characters.
Such morphological congruences indicate that the present
specimens are conspecific with "P. p/iocaenicus". Moreover, we directly compared the holotype of "P. p/iocaenicus"
with that of B. pohaiensis, and remeasured their lower molars(Table 3). Comparison and remeasurement reveal thatmorphological and size differences between them are veryslight, and the diagnostic characters of "P. p/iocaenicus"
mentioned by Flynn and Wu (1994) are not decisive for
specific distinction, when we take the Haimao specimens
into consideration. In conclusion, "P. p/iocaenicus" is synonymous with B. pohaiensis.
The Haimao specimens provide us much knowledge on
the morphology of the skull, upper teeth, anterior part ofmandible, first lower incisor and P, of B. pohaiensis as wellas the morphological variation of its mandible, all of whichwere hitherto unknown. On the basis of such knowledge,

4

o

2mm

Figure 9. Simplified sketch of the mandibular ascending rami of Beremendia pohaiensis in buccal view,comparing the holotype of "Peisorex pohaiensis" (1) with the specimens from Haimao (2-4). 1: V2671, 2: DH8956,
3: DH8951, 4: DH8957.

Chang-zhu Jin and Yoshinari Kawamura

442

2\U~11~.·.;~.;,>.~'"'--G#'.

.

.•. . . .

. C~'~··.:·,,<j:. .......8o

2mm'-----'-----'

Figure 10. Simplified sketch of the mandibular ascending rami of Beremendia pohaiensis in lingual view,comparing the holotype of "Peisorex pohaiensis" (1) with the specimens from Haimao (2-4), and showing thecharacteristic parts (A-C). 1: V2671 , 2: DH8956, 3: DH8951, 4: DH8957. A: anterior lean of the coronoid
process, B: size of the mandibular foramen, C: shape of the lower part of the condyle.

3i2.. 1tf,.-I• • '·t;..::

upf' .

ps.

o

:' uf

1mm

'--'-'

Figure 11. Simplified sketch of the mandibular ascending rami of Beremendia pohaiensis in dorsal view,comparing the holotype of "Peisorex pohaiensis" (1) with the specimens from Haimao (2-4). 1: V2671, 2: DH8956,
3: DH8951, 4: DH8957. itt: internal temporal fossa, Ipc: lower part of the condyle, ps: pterygoid spicule, uf:
upper facet, upf: upper pterygoid fossa.
3

Figure 12. Simplified sketch of the mandibular condyles of Beremendia pohaiensis in ventral view, comparing
the holotype of "Peisorex pohaiensis" (1) with the specimens from Haimao (2-4). 1: V2671 , 2: DH8956, 3:
DH8951, 4: DH8957. ia: interarticular area, If: lower facet, mf: mandibular foramen, uf: upper facet.

we compare B. pohaiensis with the species of Beremendia
hitherto described.
Reumer (1984) listed the four species as members of thegenus: B. fissidens, "B. sinensis", B. ucrainica and B. minor.
B. ucrainica is probably con specific with B. fissidens as
already mentioned, and "B. sinensis" cannot be included in
the genus as discussed below. Thus, B. fissidens and B.
minor are important for comparison to B. pohaiensis. B.
fissidens is generally similar to B. pohaiensis in the morphology of the skull, mandible and dentition, but the following
differences are also observed; in B. fissidens, the externalnaris is more slender (Sulimski, 1959; fig. 4), the depression
behind the first upper incisor terminates more posteriorly on
the lateral wall of the rostrum (Sulimski, 1959; RzebikKowalska, 1976), A4 is always present, the buccal cingula ofthe lower molars are generally thicker and less undulated,
and the mandibular foramen is more variable is size. We
cannot evaluate wheather the first and second differences
represent species level or individual variation, because thespecimens described in the above-mentioned literature arefew. On the other hand, the third difference is more decisive because in B. pohaiensis N is completely lacking, while1010.

First reliable record of Beremendia

the literature has shown the presence of A 4 in B. fissidens on
the basis of sufficient numbers of specimens. We consider
that other differences are also specific, although they are
subject to individual variation.
As regards size, B. fissidens shows a wide range of

443

variation (Sulimski, 1962; Rzebik-Kowalska, 1976; Reumer,1984). The measurements of B. pohaiensis are plotted wellwithin the range of B. fissidens, toward the larger end of therange.
As described by Rzebik-Kowalska (1976) and Reumer

Figure 13. Geographic distribution of Beremendia. • = representative fossil locality, 0 = questionable recordin East Asia.
1: Sugworth (Stuart, 1980), 2: Courterolles (Brochet et at., 1983), 3: Valerots (Chaline, 1972a, b), 4: SaintSauveur (Crochet and Michaux, 1981), 5: Mas Rambault (Chaline, 1972b), 6: Brielle (Meulen and Zagwijn, 1974),7:
Tegelen (Reumer, 1984), 8: Hohensulzen (Heller, 1962; Storch et at., 1973), 9: Upper Terrace of the River Werra(Heinrich, 1982), 10: Sackdillinger H6hle (Heller, 1930) and Deinsdorf (Heller, 1963), 11: WeiBenburg 7 (Koenigswald,1971) and Schernfeld (Dehm,1962), 12: Arondelli (Berzi et at., 1970), 13: Soave (Maul, 1990), 14: Monte Peglia(Meulen, 1973), 15: Podumci 1 (Maul, 1990), 16: Chlum (Fejfar and Hora~ek, 1983), 17: Stranska skala (RzebikKowalska, 1972), Hol~tejn (Musil, 1966; Fejfar and Hora~ek, 1983) and Mokra (Fejfar and HorEi6ek, 1983), 18:
Ivanovce (Fejfar, 1966) and Skalka (Maul, 1990), 19: Kolinany (Fejfar and Hora~ek, 1983), 20: Hajna~ka (Fejfar,1964), 21: Ple~ivec (Fejfar and HorEi6ek, 1983), Gombasek (Maul, 1990) and V~elare (Fejfar and Hora~ek, 1983;
Hora~ek, 1985), 22: Deutsch-Altenburg (Mais and Rabeder, 1977), 23: Dunaalmas (Janossy, 1986), 24: Villany(Kormos, 1934; Kretzoi, 1956; Reumer, 1984; Janossy, 1986), Beremend (Kretzoi, 1956; Janossy, 1986), Nagyharsanyhegy (Kretzoi, 1956), Csarn6ta (Kretzoi, 1956, 1959; Reumer, 1984) and Somssich Hill (Janossy, 1986), 25:
Tark6 (Janossy, 1962,1969,1986), 26: Osztramos (Janossy and Kordos, 1977; Reumer, 1984; Janossy, 1986), 27 :Betfia (Terzea and Jurcsak, 1968; Terzea, 1973), 28: Chi$c8U (Maul, 1990), 29: W~ze, R~bielice Kr61ewskie andZalesiaki (Rzebik-Kowalska, 1976), 30: Kamyk (Kowalski, 1960), 31: Kielniki and Zamkowa Dolna (RzebikKowalska, 1976), 32: Kadzielnia (Kowalski, 1958; Rzebik-Kowalska, 1976) and Kozi Grzbiet (Rzebik-Kowalska,1976), 33: Zabia Cave (Bosak et at., 1982), 34: Chertkov (Pidopli~ko, 1956) and Gorishnya Vygnanka (Maul, 1990),
35: Uryv (Agadjanian, 1977), 36: Razdol'e (Zazhigin, 1980), 37: Yushe Basin (Flynn and Wu, 1994; this paper),38: Chiachiashan (Kowalski and Li, 1963; this paper), 39: Haimao (this paper), 40: Beregovaya (Erbajeva; per.
comm.), 41: Bilike (Qiu and Qiu, 1995), 42: Nihewan (Cai, 1987), 43: Zhoukoudian (Kretzoi, 1956)

Chang-zhu Jin and Yoshinari Kawamura

444(1984), the morphology of B. minor is identical with that of B.
fissidens, but B. minor is decidedly smaller than B. fissidens.
The metrical data given by these authors clearly indicate that
B. minor is much smaller than B. pohaiensis.
Discussion.-Fossil localities of Beremendia, hitherto
known, are concentrated in Europe (Figure 13). In East Asia,
however, only three records are present in the literature.
They are from the Middle Pleistocene at Locality 1 ofZhoukoudian (= Choukoutien), from the Late Pliocene in the
Nihewan Basin and from the Early Pliocene of Bilike. The
first one is represented by only one mandible described byZdansky (1928) as a new species of Neomys, UN. sinensis".
Subsequently, Kretzoi (1956) transferred this to Beremendia,
and this opinion was followed by Sulimski (1959) and Repenning (1967). On the other hand, Kowalski and Li (1963)
provided the different view that "N. sinensis" did not belong
to Neomys and also differed from Beremendia. On the basisof the description and figures given by Zdansky (1928), thelatter view is more reasonable, because "N. sinensis" isdistinct from Beremendia in having the teeth unpigmented,
the mental foramen more anteriorly placed, the lower part ofthe mandibular condyle more posteriorly placed, and inhaving very weak cingula on the lower molars. Thus, we
believe that "N. sinensis" belongs to a different genus from

Beremendia. Moreover, the occurrence of "N. sinensis"
from Locality 1 of Zhoukoudian is questionable, as alreadymentioned by Young (1934) who subsequently examinedabundant material from the same locality. He stated that nofurther trace of "N. sinensis" had been obtained there and"Either, the species is exceptionally rare in Choukoutien; orsome confusion has been made by Zdansky in the locality."
Additionally, as regards soricid remains from Zhoukoudian,
Kowalski (1958) mentioned that Neomys boh/ini described byYoung (1934) was nearer to Beremendia than to Neomys.
This opinion is, however, untenable, because N. bohlini ismuch smaller and is considerably different from Beremendia
in the shape of the mandible. This species was subsequently included in Chodsigoa by Repenning (1967).
The second one from the Nihewan Basin is represented byonly three isolated molars which were assigned to "? Beremendia sp." by Cai (1987). His description does not allow
one to judge whether these molars are referable to Beremendia or other soricid genera.
The third one is the record of Beremendia very recently
mentioned by Qiu and Qiu (1995). Unfortunately, they gaveneither specific determination nor description of the specimens allocated to Beremendia. Thus, we cannot judge
whether their allocation is correct or not.

... ~ :,
I~#":;.:-,-~.,.,,"--;.:,~.·'_ ",_,:.'.'.._., . .
. \... /1··{E,'.'::·~:,. .....

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B.

".-- n./!-- /'~r/SsidellS"''-:'~ ::~'..'!·~·?--J\e~'('" /..

,::'!~ __ :,",:;\:,.".,~. ""'\

,..."

,

t'{

, ,

,; ,

"

, '

\ ~
~

:

\:

"

rr

,,

,",,

1:

\~:':,;:::,., ..
--,'-',!

"
.. :

, ,'

'"

:'

EARLY PLEISTOCENE

Figure 14.

\

:

','

Distributional history of Beremendia throughout Eurasia.

MIDDLE PLEISTOCENE

1010.

First reliable record of Beremendia

Besides these records, the possibility of the occurrence of
Beremendia from Transbaikalia is suggested by MA Erba-

jeva (personal communication). According to her, however,
the occurrence is quite controversial. At any rate, the wellpreserved specimens from Haimao, as well as the two
mandibles originally assigned to Peisorex, first demonstrate
the distribution of the genus in East Asia (Figure 13).
Between Europe and East Asia, Beremendia was recorded
from the early Pleistocene of Razdol'e, western Siberia(Zazhigin, 1980). He regarded it as a new species, but
unfortunately, he gave no description of the species in thearticle.
Beremendia first appeared in the early Pliocene of Europe,and at that time, it was already represented by two species,
B. fissidens and B. minor, which coexisted until the latest
Pliocene or earliest Pleistocene (Reumer, 1984). In the early
Pleistocene, B. fissidens became the only representative of
the genus in Europe, and survived until the middle Pleistocene there. On the other hand, B. pohaiensis from the
Yushe Basin indicates that Beremendia already inhabited
north China at least in the middle Pliocene. This possibly
resulted from its eastward migration from Europe by thattime, because its remains are more abundant and diversified
in the early and middle Pliocene of Europe. A scenario of
its distributional history throughout Eurasia is shown in Figure
14.

Conclusions
The well preserved large shrew remains obtained fromearly Pleistocene fissure sediments at Haimao are allocatedto the genus Beremendia, because they have the following
diagnostic characters: the teeth are heavily pigmented; thefirst upper incisor is markedly bifid; the posterior margins of
p4 and upper molars are moderately emarginated; thecoronoid process of the mandible leans anteriorly, and theupper pterygoid fossa is distinct; the interarticular area isvery broad, and has lingual emargination; the lower facet isplaced very anteriorly; the internal temporal fossa is deeply
pocketed; the first lower incisor has no cusplets on its
cutting edge, and its apical part is strongly bent upward; theposterolingual basin and entoconid crest are present on P4 ,and on M, and Mz, respectively.
On the other hand, the holotype of Peisorex pohaiensis,
the only specimen of the type species of the genus Peisorex,
is re-examined and compared with Beremendia fissidens,
the type species of Beremendia. The comparison reveals
that there are no basic morphological differences indicativeof generic distinction between them. Peisorex is, therefore,synonymous with Beremendia, and is preoccupied by thelatter. The species name, Peisorex pohaiensis, should be
replaced by Beremendia pohaiensis.
In comparison with the holotype of B. pohaiensis, theHaimao remains well coincide with the holotype in morphology and size. Thus, they are identified as B. pohaiensis.
Furthermore the holotype of "Peisorex p/iocaenicus" recently
described is compared with the Haimao remains and theholotype of B. pohaiensis. The comparison reveals that allof them are conspecific, and "P. p/iocaenicus" is synony-445

mized with B. pohaiensis.
The Haimao remains provide us much knowledge onhitherto unknown osteological and dental features of B.
pohaiensis. Armed with this knowledge, we can distinguishB. pohaienis from the known species of the genus in the lackof A4, and in having the mandibular foramen always large
and deep, and the buccal cingula of the lower molars thinnerand remarkably undulated.
Fossil records of Beremendia were hitherto concentrated
in Europe. Only three records of the genus were previously
known in East Asia, but they were insufficiently described.
The identification of the Haimao remains as Beremendia, as
well as the new allocation of "Peisorex pohaiensis" and "P.
p/iocaenicus" to the same genus, verifies the first reliable
record of Beremendia in East Asia.
Its occurrence in north China indicates that it was distributed in both eastern and western Eurasia from the middle
Pliocene to the early Pleistocene. We can construct a
scenario with Beremendia first appearing in the early
Pliocene of Europe, and then expanding eastward to East
Asia by the middle Pliocene, where it became extinct by theend of the early Pleistocene, while it survived until the middle
Pleistocene in Europe (Figure 14).

Acknowledgments
We are grateful to Drs. Y. Tomida of National Science
Museum (Tokyo) and L. J. Flynn of Harvard University (Cambridge) for critically reading drafts of this paper and forvaluable discussions. We also thank Professors H. Kumai
of Osaka City University, Li Chuan-kui and Qiu Zhu-ding of
the Institute of Vertebrate Paleontology and Paleoanthropology, Academia Sinica (Beijing), and Mr. H. Taruno of
Osaka Museum of Natural History for encouraging us
throughout this study and giving us useful suggestions; andMessrs. Sun Yu-feng and Liu Jin-yuan of the Dalian
Natural History Museum for collecting the Haimao remains
described here and helping us in field work.
Important information on Beremendia has been provided
from the following persons; Drs. R.-D. Kahlke and L. Maul ofFriedrich-Schiller-Universitat Jena (Bereich Quartarpalaontologie in Weimar); Dr. MA Erbajeva of Buryat Geological Institute, Russian Academy of Sciences (Ulan-Ude);
Dr. AK Agadjanian of Paleontological Institute, Russian
Academy of Sciences (Moscow).
We express our thanks to Dr. Wu Wen-yu of the Instituteof Vertebrate Paleontology and Paleoanthropology,
Academia Sinica for sharing his knowledge on soricids fromthe Yushe Basin and encouraging us in writing this paper
and to Mr. M. Fujita of Osaka City University for the preparation of the drafts.

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Beishan ~tUl, Bohai M, Chiachiashan Ji*Ul, Dalian :kit, Haimao #iij'f, Liaodong ~*, Lushun,*JI~, Nihewan l'JEr-ilJ~, Yushe tmt±, Zhoukoudian}E[jDmTrans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.448-453, 3 Figs., June 30, 1996
© by the Palaeontological Society of Japan 1996

Stable isotope records of the Pliocene fossil Akebiconcha
kawamurai (Bivalvia: Vesicomyidae) from the Tamari
Formation, Central Japan: Indication ofchemoautotrophic symbiosis
BOO-KEUN KHIM l , TAKAMI NOBUHARA2 and DAVID E. KRANTZ llCollege of Marine Studies, University of Delaware, Lewes, DE 19958, U.S.A.
2Department of Earth and Planetary Sciences, Graduate School of Science, Nagoya University, Nagoya, 464-01 Japan

Received 19 November 1995; Revised manuscript accepted 7 March 1966

Abstract Stable oxygen and carbon isotope profiles of the Early Pliocene fossil Akebiconcha kawamurai
from the Tamari Formation, Central Japan, are constructed to obtain environmental and physiologicalinformation using a series of samples from the shell surface for a high-resolution record. The 0 180 profile
indicates that hydrographic conditions were stable and similar to those of modem bathyal depths. The
isotopic temperature was estimated to be around 6 to BOC with a little seasonal variation. The 0 13C profileshows an apparently progressive by increasing trend during shell growth, a feature which has been
identified from some live mollusks containing symbiotic bacteria. Therefore, the stable isotopic geochemical profiles are regarded as potential indicators of the paleoecological habitat and symbiosis withchemoautotrophic bacteria of fossil mollusks.
Key words: Pliocene, chemoautotrophic symbiosis, stable isotopic record, chemoautotrophic bivalve,
Tamari Formation, Shizuoka, Japan
Introduction
Nobuhara and Tanaka (1993) described the molluscan
assemblage dominated by Akebiconcha kawamurai fromseveral shell beds intercalated in massive silt of the Early
Pliocene Tamari Formation, Central Japan (Figures 1A, 8).
The A. kawamurai assemblage is commonly associated with
Solemya johnsoni, Lucinoma aft. acutilineata, and Conchocele bisecta. The Japanese vesicomyid clam A.
kawamurai lives at bathyal depths on the Pacific side ofCentral Japan (Kuroda, 1943) and is taxonomically closely
related to Calyptogena species that have been observed invarious reducing environments (Arp et al., 1984; Kennicutt II
et al., 1985; Okutani and Egawa, 1985). Many living
speCies of Calyptogena, Lucinoma, and Solemya are known
to prefer reducing environments and possess endosymbiotic
chemoautotrophic bacteria which provide energy to the host
(Felbeck et al., 1981 ; Cavanaugh, 1983). On the basis of thespecies composition and its extraordinarily large biomass
compared with the oxic-environment molluscan assemblage
between the shell beds, Nobuhara and Tanaka (1993)
presumed that A. kawamurai might be sustained by a sulphide-energy-based metabolism with chemoautotrophic
symbionts.

It is generally recognized that the ol3C of soft parts in live
chemosymbiotic mollusks indicates the source of the carbon, since from an identical CO 2 source the carbon fixed bysulphide-oxidizing bacteria is more 13C-depleted than that
fixed by phytoplankton (Spiro et al., 1986). However, theidentification of a symbiotic relationship in the fossil record ismore problematic because the viscera and symbionts are notpreserved, nor do the latter produce identifiable structures in
the hard parts or skeleton of the host. Recent studies havereported stable isotope profiles from the shells of live
chemoautotrophic symbiont-bearing mollusks (Rio et al.,
1992; Oba and Hattori, 1995). Presented here are shell
oxygen and carbon isotope profiles from a specimen of thebivalve mollusk Akebiconcha kawamurai obtained from the
Early Pliocene Tamari Formation. The shell isotopic composition of this specimen by comparison with living mollusks
is used to infer a symbiotic association with chemoautotrophic bacteria in a paleoecological setting.

Geologic setting and fossil collection site
The Late Miocene and Early Pliocene Tamari Formation is
one of the late Neogene marine sedimentary units exposedin the Kakegawa area, Central Japan (Figure 1A). More than1011.

Stable isotope records of fossil Akebiconcha

449

ding. The mode of occurrence, however, implies that the
sampling point NK103 was close to the original habitat(Nobuhara and Tanaka, 1993).

Materials and analytical method
The right valve of an articulated specimen of Akebiconcha
kawamurai from the sampling point NK103 was used for thisisotopic study. The shell is more than 49.9 mm in length(the posterior and anterior ends are lost) and 39.9 mm inheight (Figure 2A). It was collected from a fresh outcrop of
massive silt at a golf driving range under construction.
This study incorporates a serial shell-sampling method toprovide a detailed stable isotope record encompassing thelife of the mollusk: this method has previously been employed successfully to assess intra-shell isotopic variability(Arthur et al., 1983; Krantz et al., 1987; Cornu et al., 1993 ;Weidman et al., 1994). Twenty-eight carbonate powder
samples were obtained from the outer shell layer along theaxis of maximum growth using a dental drill with a 0.3 mm
bur (Figure 2A). Careful sample drilling avoided penetrating
the inner shell layer. Prior to drilling, the shell exterior was
ground lightly to remove fouling organisms and any surficiallyattached materials. Approximately 0.5 mg of each carbonate powder sample was reacted with purified phosphoricacid at 90'C to produce carbon dioxide gas which was
subsequently analyzed on a VG PRISM mass spectrometer.
All isotope values are reported in 0 notation relative to the
PDB standard as below (Craig, 1965).
OISO (% )- [ eSOjlSOlsAMI'LE -esO!,sOlsTANDAHD ] X 1000
00 eSO!,sO)STANDARD
o13C (%0)== [ e3Cj'2Cls,~MPL~2-e3Cj'2C)STANDAHD ] x 1000
( Cj C)STANDARD

Figure 1. (A) Index map of the Kakegawa area. (8)Map showing the location of the sampling locality, plotted on
1 : 25,000 topographic map "Kakegawa" published by Geographical Survey Institute of Japan. (C) Mode of occurrenceof the Akebiconcha kawamurai assemblage at sampling point
NK103 (bedding plane view in a mud block excavated duringsite construction).

200 meters of massive grayish fine-grained silts were deposited in a deep-marine setting (Ishibashi, 1989). The
Tamari Formation is exposed as an inlier surrounded byturbiditic alternations of sand and silt of the Pliocene Horinouchi Formation. Sedimentary facies analyses haveshown that the Tamari Formation was deposited on the slopeof a fore-arc basin similar to the present western part of
Suruga Bay (Ishibashi, 1989; Tsukawaki, 1994).
The horizon from which specimens were collected by
Nobuhara and Tanaka (1993) is situated by Ibaraki (1986)
between Datum 11 (3.7 Ma) and Datum 18 (3.0 Ma) based on
the planktonic foraminiferal biostratigraphy. Abundant large
and small shells of mollusks inhabiting reducing environments are closely or sporadically spaced within the shell
beds and supported by a silt matrix (Figure 1C). Most of theshells lie with their commissure planes parallel to the bed-

On the basis of the reproducibility of standards and replicate analyses of samples, precision is ±0.1%0 for both OISO
and 013C.

Results and discussion
Stable oxygen and carbon isotope profiles of fossil shells
provide important paleoenvironmental information such as
annual temperature range, seasonal salinity variations, extent
of primary productivity and food sources (Chinzei and Aoshima, 1976; Krantz, 1990; Cornu et al., 1993). However,
the isotopic composition of shell carbonate may also be
influenced by internal biological effects such as the metabolic activity of symbionts (Romanek et al., 1987).
8 1sO profile: The OISO profile across the shell expresses
no significant variation (Figure 2B). This suggests that theshell carbonate was secreted under relatively uniform temperature conditions. The paleotemperature is calculated byusing the aragonite isotope temperature equation of Horibeand Oba (unpublished) as follows.
T=18.5-4.72 (o.+-o.w+)+0.12 (o.+-o.w+)2
The estimated temperature is around 6 to 8"C with a little
seasonal temperature variation. This assumes the same
isotopic composition as present seawater, because theBoo- Keun Khim et al.

450(A) Akebiconcha kawamurai

-2

---

(8)

0
0

--

0

0

0

(')

813C

~

0

co

2

~8180

~

o

10

20

30

40

Distance from umbo (mm)Figure 2. (A) Sampling positions of carbonate powders
for isotopic analyses from the fossil Akebiconcha kawamurai
specimen. Scale = 1 cm. (8) Oxygen and carbon isotope
profiles of the A. kawamurai specimen. The lack of distinct
seasonality in the 0180 profile suggests stable hydrographic
conditions during growth. The o 13C profile also displays noapparent seasonality, but becomes progressively more positive
during growth.

mean oxygen isotopic value of benthic foraminifera at ODP
site 659 between 3.0 and 3.7 Ma is nearly the same as the
Holocene level (Tiedemann et al., 1994). This interpretationof the 0' 180 profile implies that A. kawamurai lived below thedepth of the thermocline. The uniform hydrographic conditions were similar at depths greater than 400 m in presentday Sagami Bay as observed by Kawabe and Yoneno (1987).
The paleoenvironment inferred from the isotope results is
consistent with the interpretation from the fossil assemblages at the sampling locality NK103. Nobuhara (1992)
reported that the species compositions of the fossil molluscan assemblages are similar to the fauna living at intermediate water depths (600- 800 m) in Sagami Bay because bothcontain some cold- water species such as Neptunea constricta and Solemya johnsoni. In addition, the benthic foraminiferal assemblage obtained from the sampling pOint

NK103 includes many species which indicate a paleodepthof about 1000 m : Bulimina aculeata, B. striata, Sphaeroidina
bulloides, G/obobulimina auriculata, Oridorsalis umbonatus,
Bolivinita quadrilatera, and Osangularia bengalensis (Prof.
Kitazato, personal communication).
Ol3C profile : The interpretation of carbon isotope profiles
may be more problematic than for oxygen isotope profiles
because of a variety of environmental and biological influences (Grossman and Ku, 1986 ; Romanek et al., 1987).
The 0'13C profile of the Akebiconcha specimen shows a rangeof variation between - 0.86 and + 1.18%0, but displays no
obvious seasonality (Figure 2B). These values fall within therange of normal seawater isotopic composition. However,0' 13C values become increasingly more positive throughgrowth, which suggests that biological processes may beaffecting the O' 13C values for this shell. If the primary carbon
source of the Akebiconcha shell is the dissolved inorganiccarbon (DIG) of ambient seawater, the lack of seasonality inthe 0' 13C profile in part reflects that O' 13CDlC of seawater was
almost uniform during growth. In contrast, 0' 13C profiles ofnon- symbiotic mollusks living in shallow seas generally show
an apparent seasonality related to the intensity of primary
productivity in the water column (Arthur et al., 1983 ; Krantz
et al., 1987). Therefore, the habitat of Akebiconcha
kawamurai may have been somewhere beyond the seasonal
influence of phytoplankton blooms in surface water, as
would be also expected from the 0' 180 profile.
Figure 3A summarizes previously published stable oxygenand carbon isotope values from several chemosynthetic
bivalves. The relatively narrow range of 0' 180 values should
be largely dependent on the ambient water temperature at
the time of carbonate secretion on the basis of oxygenisotopic equilibrium (Epstein et al., 1953). In contrast, therange of 0' 13C values is large. Anomalously lighter carbon
isotope values for fossil Calyptogena collected from Pliocene
strata on the Miura Peninsula, Central Japan, were causedby isotopically extremely light CO 2 gas derived from respiration (Niitsuma et al., 1989). On the other hand, Kulm et al.
(1986) noted that the cold - seep bivalve Calyptogena from off
the coast of Oregon incorporates most of its carbon from theseawater bicarbonate reservoir. The O' 13C values of thisstudy are similar to those observed by Kulm et al. (1986) andOba and Hattori (1995). Biological effects of chemosymbionts on the isotope values are not clearly characterized asshown in Figure 3A. However, a progressive trend ofincreasingly more positive 0' 13C values similar to our results
has been reported from some live chemosymbiotic molluscan shells (Figure 3B). Rio et al. (1992) showed a gradualrise of the mean 0'1 3C from both Bathymodiolus thermophilus
living in the hydrothermal vent of the East Pacific Rise andCodakia orbicularis in shallow- water reducing muds of theGreat Bahama Bank. In addition, Calyptogena soyoae living
in a cold- seep region of Sagami Bay also exhibits a progressive increase of 0'1 3C values during ontogeny (Oba andHattori, 1995).
There has been no clear explanation for this progressive
increase of 0' 13C values during shell growth. Rio et al. (1992)
noted that the carbon source in the extrapallial fluid of achemosymbiotic mollusk is a mixture of seawater bicarbon-

1011. Stable isotope records of fossil Akebiconcha

451

5 .-----------------------~

(A)

-3

(8)

-1

0
.--.
0

--

-....0
0
()

O?~

0 '"

Calyptogena soyoae

-5 -

.--.

C')

~

vo
\l

<>

-10

{}.
o

o
o

3

This studyro
Rio et al. (1992)
Ci:J
Kulm et al. (1986)
Niitsuma et al. (1989)
Oba and Hattori (1995)
Dando and Spiro (1993)

5-15 ---'---,-~------,---__,_--I
-2

o

-0
0

4

7

6 0

50

100

150

200

Distance from umbo (mm)Figure 3. (A) Scatter plots of 0180 vs 013C values previously reported for chemosynthetic mOllusks. There isno clear characterization between 0180 and 013C on the biological effects of chemosymbionts. (B) Carbon isotope
profiles of chemosymbiotic shells, Bathymodiolus thermophilus sampled in the vicinity of a hydrothermal vent,Codakia orbicularis from the Great Bahama Bank (Rio et al., 1992) and Calyptogena soyoae from Sagami Bay (Obaand Hattori, 1995). Note the progressive increase of 013C during the growth of mollusks.

ate, which can migrate through the mantle or pallial edge,
and respiratory CO 2 from the chemosynthetic bacteria andthe bivalve itself. The respiratory CO 2 has much lighter 0 13C
values than ambient seawater (Tanaka ef al., 1986; Niitsuma
ef al., 1989). Several authors have documented that an
ontogenetic depletion in 013C values was due largely tochanges in metabolism with age (Krantz ef al., 1987;
Romanek ef al., 1987). If a significant part of the metabolic
CO2 is incorporated into the shell during formation, theisotopic composition of the shell carbonate would be lighter
than equilibrium values. However, in this study the 013C
profile of Akebiconcha kawamurai shows an inverse patternwith increasing 013C values through ontogeny (Figure 28).
For an explanation of this positive trend in the 013C profile,
Rio ef al. (1992) proposed the following hypothesis. The
sulphide-oxidizing bacteria take up a portion of the dissolved
inorganic carbon from the extrapallial liquid for theirbiosynthesis. A large isotopic fractionation arises in thismetabolic uptake process. The chemosynthetic bacteria
selectively extract light carbon (12C) leading to high concentrations of 13C in the extrapallial liquid, which is subsequently
used in shell formation. The progressive 0 13C increase may
be controlled by the following factors: (1) metabolic activity(extraction) of the symbiotic bacteria gradually increased
during the shell growth; and (2) shell carbonate secretion
decreased in later growth stages relative to the rate ofbacterial metabolic extraction.
Another interpretation is based on the measurement ofdifferent isotopic ratios from different parts of the same shellsurface (Niitsuma ef al., 1989; Oba and Hattori, 1995). Oba
and Hattori (1995) reported that carbon isotope values of theventral part of a cold-seep bivalve, Calypfogena soyoae,
differ by ca 2 %0 from portions of the shell below and above
the sediment surface. C. soyoae changes its life position
from infaunal to semi-epifaunal during shell growth (Horikoshi and Hashimoto, 1993). Such a change of habitat could
result in the isotopic change. The life position of Akebiconcha kawamurai has not been directly observed. More datafrom isotope profiles and more information on life position arenecessary to confirm this hypothesis.
The stable isotope profiles constructed from Akebiconcha
kawamurai are consistent with the paleoecology interpretedby Nobuhara and Tanaka (1993). A. kawamurai is inferred tohave lived in a stable bathyal habitat and possessed endosymbiotic sulphide-oxidizing bacteria. However, thecause of reducing conditions in the ecosystem of the
Akebiconcha community is unclear; cold seeps or a hypoxic
water mass caused by restricted circulation are both probable. Nobuhara and Tanaka (1993) inferred that the occurrence of a reducing environment was related to a dissolvedoxygen minimum at bathyal depths. Alternatively, Kanie ef
al. (1992) reported calcareous siltstones and lenticular-shelly
limestone from the same studied area. They suggested thatcalcification was dominantly controlled by methane seepage.
Therefore, further studies on the isotopic composition ofauthigenic carbonate are needed to determine the environmental settings of these reducing environments.
Conclusions
Stable oxygen and carbon isotope profiles of the Early
Pliocene fossil Akebiconcha kawamurai from the TamariBoo-Keun Khim et al.

452

Formation, Central Japan, provide the following paleoenvironmental and paleoecological information.
(1) Both oxygen and carbon isotope profiles show noapparent seasonality. The estimated isotopic temperaturefrom 0 180 values and small seasonal variations imply that A.
kawamurai lived in a stable bathyal habitat below the depthof the thermocline. An analogous setting would be atintermediate water depth of the present Sagami Bay.
(2) The 013C profile exhibits a trend towards progressively
more positive values during shell growth. The same characteristic has been identified from some live mollusks
containing chemosymbiotic bacteria. According to Rio etal. (1992), this isotopic feature reflects the role of symbiotic
sulphide-oxidizing bacteria which preferentially extract lightcarbon from the extrapallial liquid for biosynthesis.

Acknowledgments
This research was supported in part by the Petroleum
Research Fund of the American Chemical Society (Grant
27567 -AG). We thank Dr. Craig Cary (University of Delaware) for a critical review and discussion of our final draft.
We also thank Dr. T. Ozawa (Nagoya University) and Prof. T.
Oba (Hokkaido University) for valuable comments and helpful
suggestions. Thanks are also due to Prof. H. Kitazato(Shizuoka University) for information on the benthic foraminiferal assemblage of the studied locality.

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mill, Tamari m*Trans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.454-466, 10 Figs., June 30, 1996
© by the Palaeontological Society of Japan 1996

Laboratory observations of sexual and asexual
reproduction of Trochammina hadai Uchio
HIROSHI KITAZATO and SATOSHI MATSUSHITA
Institute of Geosciences, Shizuoka University, Oya 836, Shizuoka, 422 Japan
Shin-Nippon Meteorological and Oceanographical Consultant Co. Ltd.,
2-2-2 Hayabuchi, Tsuzuki Yokohama, 224 Japan

Received 30 November 1995; Revised manuscript accepted 23 February 1996

Abstract Trochammina hadai Uchio is abundant in brackish water bays around the Japanese Islands andexhibits a biphasic life cycle in natural environments. In the laboratory sexual reproduction, characterized
by the release of thousands of gametes, occurred in spring. The release of gametes continued for 1.5
hours. After gametogenesis, parts of the cytoplasm still remained in the mother test. Asexual reproduction took place in the laboratory during autumn and continued for 6 hours. The mother test was not
destroyed during asexual reproduction. The geographical distribution of T. hadai in Hamana Lake differsfrom season to season. This may be explained by the differential dispersal of juveniles during the sexualand asexual phases, which take place at different times of the year.
Key words: Reproduction, biphasic life cycle, microspheric and megalospheric generations, geographic
distribution, Trochammina hadai

Introduction
Recently, agglutinated foraminifers have become one of
the important groups in the study of extreme environments
such as the deep sea and brackish waters (Hessler andJumars, 1974; Bernstein et a/., 1978; Bernstein and Meador,
1979; Gooday, 1986,1988,1990; Gooday and Lambshead,
1989; Schroeder et a/., 1988). Foraminiferal biomass may
be significant in such environments, e.g., accounting for up
to 50% of the total biomass in the deep sea (Snider et a/.,1984). Foraminifers also may act as an important factor in
the deep-sea carbon budget (Gooday et a/., 1992). The
foraminiferal fauna below the calcite compensation depth(CCD) is composed entirely of agglutinated species. Thus,
biological information about agglutinated foraminifers is
required for understanding deep-sea biology, ecology andbiogeochemical cycles.
Agglutinated foraminifers are also widely distributed incoastal regions. They are good indicators for monitoring
polluted environments (Alve, 1991). In this case as well,study of the biology of agglutinated foraminifers is important
for an understanding of modern ecological processes.
However, investigations of the biology and ecology of agglutinated foraminifers are scarce even for shallOW marine
environments in comparison to calcareous foraminifera(Boltovskoy, 1966; Matera and Lee, 1972; Salami, 1976;
Sliter, 1968; Angell, 1980,1990).
Trochammina hadai Uchio is an agglutinated foraminifer

that is abundant in brackish waters of Japan (Ishiwada, 1958 ;Uchio, 1962a, b; Ikeya, 1970,1977; Matoba, 1970). This
species, together with Ammonia beccarii (Linne), accounts forthe greater portion of the foraminiferal population in brackish
waters.
To understand the life history of T. hadai, we observed
almost continually the seasonal changes of populations at a
fixed station in Hamana Lake, Central Japan, from 1988
through 1990. The biphasic life cycle was inferred from theseasonal occurrences of the natural populations (Matsushita
and Kitazato, 1990). To examine our investigations undernatural conditions we cultured T. hadai in the laboratory.
During the course of this culture experiment, both sexual andasexual reproduction were observed. Here, we describe thereproductive processes of T. hadai in detail.

Method of study
Culture studies were carried out at the Fisheries Laboratoryof the Faculty of Agriculture, University of Tokyo at Maisaka,
which faces Hamana Lake in Shizuoka Prefecture, Japan.
Sediment samples for culture were collected by SCUBA
diving from a fixed station in the Shonai Inlet of Hamana
Lake, where we observed almost continually the seasonaloccurrences of natural populations of T. hadai (Matsushita
and Kitazato, 1990). Sediments were transported with ambient sea water to the laboratory. Living individuals were
picked from the sediments and transferred to a petri dish

1012. Reproduction of Trochammina hadai

Figure 1. Successive photographs of sexual reproduction. Time of photographic exposure is given in theupper left comer of each photograph. All photographs were taken on March 20, 1990. 1. Release of gametes.
x 25.4. 2. Clusters of gametes rising up from aperture. x 50.8. 3. Clusters of gametes. x 38.1. 4. Clusters ofgametes. x 38.1. 5. Clusters of gametes. x 25.4. 6. Clusters of gametes. x 38.1

455

456

Hiroshi Kitazato and Satoshi Matsushita

Figure 2. Successive photographs of sexual reproduction. Time of photographic exposure is given in theupper left corner of each photograph. All photographs were taken on March 20, 1990. 1. Release of gametes.
x 25.4. 2. Release of gametes. x 38.1. 3. Release of gametes mostly completed. x 50.S. 4. End ofgametogenesis. x 25.4. 5. Beginning of extrusion of rhizopodia. The end of rhizopodia are rounded and creep
shaped. X 76.2. 6. Extrusion of many rhizopodia and movement of foraminifer. X 38.1

1012. Reproduction of Trochammina hadai
using a pipette. Individuals were cleaned with filtered sea
water by transferring from one dish to another repeatedly.
Each individual was put in a petri dish for culture. Bothdried green algae of the genus ChIarella and living diatomsof the genus Navicula served as foods. Diatoms were
supplied by the fisheries laboratory. Small amounts ofcarborundum particles were added to a petri dish instead ofusing natural sediments. All petri dishes were placed in alaboratory at room temperature (15- 18"C) and were exposed
to natural light through laboratory windows. Bottom waters(salinity : 28%0) collected at the fixed station was used for
culture. Cultures for observing sexual reproduction werecarried out from March 14 through 24, 1990. Cultures for
asexual reproduction were performed during the period from
October 26 to November 9, 1990. The periods for observations were determined from the population dynamics data ofnatural populations of T. hadai, which were continuallymonitored at a fixed station in the Shonai Inlet (Matsushita
and Kitazato, 1990).
The reproductive processes were observed with a phase
contrast apparatus attached to an inverted microscope(Nikon Diaphoto TMD and Olympus IMT - 2). Bothgamogony and agamogony were recorded on Kodak Plus- X
film and video tapes respectively.
Reproductive process
Sexual reproduction : Sexual reproduction occurred only inspring. Seven of the 30 adult individuals reproduced sexually in March. One individual reproduced in May. Sexual
reproduction took place around half moon in March, and justone day after full moon in May. No asexual reproduction
occurred in culture during the spring season.
Sexual reproduction progressed as follows (Figures 1 and
2).

1) Prior to reproduction, mature individuals that exhibited
dark orange cytoplasm withdrew their rhizopodia except forrhizopodia needed to anchor the test at the bottom. During
sexual reproduction no reproductive cyst was constructedaround the mother tests.
2) Release of gametes took place twice. At first,
gametes were released from the aperture (Figures 1-1 and- 2). Then, several clusters of gametes were extruded (Figures 1- 5 and - 6), and the second release of gametes occurred explosively 15 minutes later (Figure 2- 1). The morphology of each gamete is droplet- like in outline and consists of
two flagellae, based on light microscope observations. A
sketch of gametes is drawn in Figure 8. However, morphologic details of the gamete have not yet been elucidated
under an electron microscope.
3) Release of gametes continued for 1.5 hours. The
mother test did not move ' during reproduction and thegametes dispersed quickly. We did not observe zygote
formation.
4) After the release of gametes a part of the cytoplasm
still remained within the mother test and slowly rhizopodia

ELl Sexual reproduction
D!i Asexual reproduction

5457(Spring)(Autumn)

(f)

cU

4

:::J

"'0

>

-g 3

o

~

2

<l)

.0

E
:::J

1

Z

o

70
40
50
60
20
30
Proloculus diameter of parent individuals ( JJm )10

Figure 3.

Proloculus diameters of mother tests that reproduced in laboratory c ultures.

458

Hiroshi Kitazato and Satoshi Matsushita

extruded again from the aperture, and the test moved away
(Figure 2- 6).
All individuals that released gametes had a large
proloculus, ranging from 40 to 55,um in diameter (Figure 3).
Test diameters of mother individuals ranged from 383 to 540,um (Table 1a).
In order to obtain zygotes we mixed gametes of two
different mother individuals. However, they did not form azygote within the culture. The gametes were very difficult
to maintain under culture conditions, as they died within aday.
Asexual reproduction : Asexual reproduction took place inautumn. Eleven individuals among 30 adults reproduced
asexually within our culture. Reproduction took place
within three days after full moon. No sexual reproduction
was observed in autumn.
The reproductive process progressed as follows.
1) Reproductive cyst formation : A reproductive cyst, formed from chlorella cells and/ or diatom frustules, was constructed around the mother test, leaving vacant spaces(Figure 4). During construction of the cyst, the individuals
extruded radially many rhizopodia along the bottom of thepetri dishes to collect material to form the cyst. Thisrhizopodial pattern used during construction of the cyst isdifferent from the usual pattern. Usually, T. hadai extrudes
rhizopodia mainly in front of (i.e., in the direction of movement) and behind the test (Figure 5).
2) Cytoplasm invades the reproductive cyst : One or twohours after the reproductive cyst was constructed, thecytoplasm spread slowly into the cyst and the space wasfilled with cytoplasm.
3) Multiple division : Multiple division occurredsynchronously within the cyst cavity and within the mothertest (Figure 6-1). First, the velocity of cytoplasmic streaming

Table 1. Test diameters and proloculus diameters ofmother tests with regard to sexual and asexual reproduction.
1a. Individuals participating in sexual reproduction. 1b.
Individuals participating in asexual reproduction.
Table 1a. Individuals participating in sexual reproduction

Specimen no.
1
2
3
4
5
6
7
8

Test diameter
(,um)

478
420
447
383
505
435
457
540

Proloculus
diameter
(,um)

41
46
46
42
48
42
?
55

Table 1b. Individuals participating in asexual reproduction
Specimen no.

2
3
4
5
6
7
8
9
10
11

Test diameter
(,um)

407
459
425
507
489
533
451
422
486
441
425

Proloculus
diameter(,u m)

28
33
31
32
26
25
32
?
26
20
30

Figure 4. Reproductive cysts were constructed around a mother test during asexual reproduction. The
photograph was taken on November 3, 1990. x 25.4.

1012. Reproduction of Trochammina hadai

459

Figure 5. Usual rhizopodial extrusion of Trochammina hadai. Rhizopodia were extruded in two directions.
The photograph was taken on October 27, 1990.

accelerated and then multiple division occurred within a few
minutes. Fifty to one hundred gamont juveniles were visible
both in the reproductive cyst and in the mother test 15
minutes after the division.
4) Spreading of juvenile individuals: Mostly one or twohours after multiple division, juvenile gamonts started toleave the mother test (Figure 6- 2, - 3 and - 4). Juvenile
individuals are spherical without an arenaceous wall (Figure6- 5 and - 6). The diameters of juvenile gamonts ranged
from 45 to 65,um. This is the same as the proloculus
diameters of megalospheric adults (Figure 3). Immediately
after juveniles left the mother test, they started to collect
both ChIarella cells and diatom frustules.
5) Formation of an agglutinated test: One or two hours
after juveniles had left the mother test, most individuals
started to collect carborundum grains to form an arenaceouswall. At first, the individuals gathered any particles aroundthe cell and fixed them on the first chamber wall (proloculuswall), after which the foraminifers grabbed selectively carborundum grains that had been placed to one side. Thisshows that Trochammina hadai definitely discriminates carborundum grains from other biogenic particles. Carborundum grains were cemented first on one side of the cell andthen their use gradually extended around to the other side
(Figure 7). This means that the test formation of agglutinated foraminifera probably starts from one point. This observation of the initiation of chamber formation is similar to thedescription by Bender (1992) for Textularia candeianad'Orbigny. Nearly the same chamber formation process
was described by Angell (1990) for Trochammina inflata.
Asexual reproduction continued for approximately 6 hours.
The mother test was not destroyed during asexual reproduction, as observed by Salami (1976) for T. cf. T. quadrilaba
Hoeglund. However, the mother test was weakened andfragile after reproduction.

The proloculus diameters of mother tests that released
gamonts were smaller than those of the gamonts. They
ranged from 20 to 33 ,u m (Figure 3). Test diameters of themother tests ranged from 407 to 533,um (fable 1b).

Discussion
Both sexual and asexual reproduction took place during
specific seasons (Figure 8). Sexual reproduction occurred
only in spring and asexual reproduction during autumn. No
exceptions have been observed. The observations support
well our previous observations that the life cycle of T. hadai
is biphasic and annual (Matsushita and Kitazato, 1990).
What fundamental factors control seasonal timing of reproduction? Dissolved oxygen and temperature of Hamana
Lake bottom waters are roughly the same in spring andautumn during the two types of reproduction, suggesting
there may be some connection between these variables andphysiological cues or limits to reproduction . Water temperature at Hamana Lake fluctuates seasonally between about
6 and 2TC, but the spring and autumn periods of reproduction both fall within the limited temperature range of 13- 18°C
(Figure 9). The dissolved oxygen content of the bottom
water both in spring and autumn is about 5- 8 mill, restrictedcompared with the annual range of <2 to ) 10 mill. Thus,
reproduction may take place under conditions of approximately 15°C and 6 mill in dissolved oxygen. We could not
find a direct relationship between water salinity and reproductive season, as seasonal salinity changes can fluctuatefrom year to year, largely due to variable precipitation rates.
Nutrient conditions also do not seem to be one of thecontrolling factors of reproduction. Seasonal chlorophyll- a
concentration in the Shonai Inlet shows that phytoplankton
production was high throughout the year, although activity
was slightly lower in spring and autumn (Anil et al., 1990).

Hiroshi Kitazato and Satoshi Matsushita

460

17:15 .

'.1 7:59

j

17: 59 .
" '.

•

0 /

•

,?

0 0

.chlarella0/f '- . ... ., .'. Y \".
'.;.

o · ~ ...

0

di arom

Figure 6. Successive photographs of asexual reproduction. Time af photographic exposure is given in theupper left corner of each photograph. All photographs were taken on November 4, 1990.
1. Construction of blood cyst. X 32. 2. Gamont individuals. X 20. 3. Gamonts depart from cyst under phase
contrast. X 50. 4. Enlargement of gamonts showing rh izopodia extruding from each gamont under phase contrast. X 90. 5. Gamonts depart from cyst. X 50. 6. Gamont collecting Chlorella cells and diatom frustules forfood. - X 96.

1012. Reproduction of Trochammina hadai

461

Figure 7. Gamont juveniles collecting carborundum grains for constructing a test wall. The upper hemisphere of each cell is covered by carborundum grains. Time of photographic exposure is given in the upper left
corner of each photograph. Prior to this stage, multiple division had occurred at 9: 30 on November 5, 1990.

Nutrient levels are thus likely sufficient at all times.
In some organisms there is a temporal relationshipbetween reproduction dates and the lunar cycle. Sexual
reproduction mainly took place around half moon. Asexual

reproduction occurred within three days after full moon,which may be comparable to the reproduction cycle of someplanktonic foraminifers (Spindler et al., .1979; Bjima et al.,1990). Further research is needed, including experimental

462

Hiroshi Kitazato and Satoshi Matsushita

Megalospheric generation

·
.
ci
.
.

.
. ,.

~

•

..... .
"

~:

• ' d

"

'. ',"".'.

.,

gamontwinter1

agamont

Microspheric generation
Figure 8. Integrated life cycle of T. hadai Uchio in relation to seasons.
of Matsushita and Kitazato (1990).

cultures, in order to clarify the nature of ambient factors thatinduce or control reproduction.
The asexual reproduction process of T. handai is mostly
the same as that in T. inflata (Angell, 1990). However, theduration of reproduction is different in the two species.
Trochammina hadai took about 6 hours, whereas Trochammina inflata required ca. 24 hours (Angell, 1990).

The figure is revised from figure 15

Juvenile individuals of T. hadai consist of only one chamberwhen they leave the cyst. However, both T. inflata (Angell,1990) and T. ct. T. quadriloba Hoeglund (Salami, 1976) have
2-3 chambers at the time when the juveniles left the mothertest, the same as most investigated calcareous foraminifera
such as Ammonia beccarii (Linne), Elphidium crispum (Linne),
Pararota/ia nipponica (Asano), Glabratella spp., Bolivina spp.,

1012, Reproduction of Trochammina hadai

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Figure 9, Seasonal changes of water temperature, salinity, dissolved oxygen and thickness of oxygenatedlayer in the sediments at a fixed station at Hamana Lake during 1988 through 1990, Solid lines show the values
for bottom water just above the sediment-water interface, Broken lines show surface conditions, Shaded areashows the main reproductive seasons,Hiroshi Kitazato and Satoshi Matsushita

464

June

NovemberoFigure 10. Geographical distribution of T. hadai in June and November, 1990, at the Shonai Inlet, Hamana
Lake. Open circles show the stations where T. hadai was not found. Closed circles indicate the stations where
T. hadai were found. Histograms show size distribution of T. hadai at each station. Open bars of the histograms
beside the stations show the number of dead individuals; closed bars show the number of living individuals. L is
the number of living individuals per 10 cm 2 •and others (Kitazato, unpublished observations).
We observed that Trochammina hadai collected carborundum grains and cemented the grains, using an organic
cement, to the surface of gamont cells to construct anagglutinated test. Bender (1992) proposed six constructional stages during chamber formation for agglutinatedforaminifera that secret calcitic cement. We probably observed only initial parts of the chamber formation process.
It is probable that chamber wall construction by gamont
juveniles is a mixture of stages 1 through 3 of Bender (1992),
though in our observations gamont juveniles simply construct
an agglutinated wall on the cell surface without actuallyforming a new chamber. Further studies are needed forcorrelating correctly our observations, including constructional stages of chamber formation, with those of
Bender (1992).
The seasonal distribution of this species may reflect themode of reproduction in T. hadai. Microspheric agamont
generations of T. hadai are spread widely throughout the inlet
in June. The megalospheric generation was dispersed in
November. However, the distributional ranges of themegalospheric generation was narrower than those of the
microspheric generation (Figure 10). These variations in theseasonal distribution of T. hadai might be explained by thedifference in modes of dispersion in the sexual and asexual
progeny of this species. Agamont juveniles can disperse
widely during sexual reproduction because the gametes areable to swim of float in the water. In contrast, gamontindividuals tend to be concentrated in a rather narrow areain the lake, because gamont juveniles disperse only byrhizopodia in and on sediments. The average moving
velocity of T. hadai is 14,um/minute (Kitazato, 1981). Thismeans that T. hadai is able to migrate only 2 cm per day.
A widespread distribution may be advantageous for keeping high survival rates under stressful summer abiotic conditions, which include bottom anoxia due to strong watercolumn stratification (Matsushita and Kitazato, 1990). During summer the density of living T. hadai individuals
decreases drastically throughout the inlet. Surviving
agamonts reproduce asexually in autumn. This means thata relatively small numbers of agamonts found the succeeding gamont generation.

1012.

Reproduction of Trochammina hadai

Acknowledgments
We are grateful to K. Chinzei, Ch. Hemleben and 0.8. Scottfor. constructive suggestions and warm encouragement
dUring the course of this study. Ch. Hemleben and R.M.
Ross provided valuable comments on the manuscript. We
are also indebted to the staff of the Fisheries Laboratory,
Faculty of Agriculture, the University of Tokyo for their kind
help during our use of their laboratory. An anonymous
reviewer provided valuable comments on the manuscript.
This research was supported by Grants-in-Aid from the
Ministry of Education, Science, and Culture of Japan (nos.
61480027 and 02454028).

References cited
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1-19.
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Journal of Foraminiferal Research, vol. 10, no. 2, p.89101.
Angell, A.M., 1990: Observations on reproduction and juvenile test building in the foraminifer Trochammina inflata.
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structure, standing stock, texonomic composition,
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demic Publishiers, Netherlands.
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the species response. Marine Ecology Progress
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The role of benthic foraminifera in deep-sea food webs
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Matera, N.J. and Lee, J.J., 1972: Environmental factors
affecting the standing crop of foraminifera in sublittoraland psammolittoral communities of a Long Island saltmarsh. Marine Biology, vol. 14, p. 89-103.
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Trochammina hadai Uchio in Hamana Lake, Japan. In,
Hemleben, Ch., Kaminski, M.A., Kuhn!, W. and Scott,D.B. eds., Paleoecology, Biostratigraphy, Paleoceanography and Taxonomy of Agglutinated Foraminifera, p.
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Hiroshi Kitazato and Satoshi Matsushita

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Trans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.467-477, 5 Figs., June 30, 1996

© by the Palaeontological Society of Japan 1996

1

1013

1

Taxonomy and distribution of the subfamilyAncistrolepidinae (Gastropoda: Buccinidae)
from the Plio-Pleistocene of JapanKAZUTAKA AMANO\ MIKIKO UKITA2 and SHINJI SAT03
IOepartment of Geoscience, Joetsu University of Education, Joetsu, Niigata Prefecture, 943 Japan
2Graduate School, Joetsu University of Education, Joetsu, Niigata Prefecture, 943 Japan
3/nakadate-mura, Minamitsugaru-gun, Aomori Prefecture, 038-11 Japan
Received 7 December 1995; Revised manuscript accepted 23 February 1996

Abstract Four species of Ancistro/epis and one of C/inopegma are newly obtained and described from
Plio-Pleistocene strata in the Japan Sea borderland: Ancistro/epis masudaensis Nomura, A. grammatus(Dall), A. sp. aff. A. hikidai (Kuroda), A. sp. and Clinopegma borealis Tiba. Among the ten species of PlioPleistocene Ancistrolepidinae, A. masudaensis. A. peulepsis, A. koyamai and C. tragilis are extinct. The
first three species belong to the Ancistro/epis eucosmius group now living in the eastern North Pacific.
They suffered extinction during the late Pleistocene cold-climate maxima because of their distribution
being restricted to the Japan Sea borderland. On the other hand, in addition to occurring in the PlioPleistocene in the Japan Sea borderland, A. grammatus, C. borealis and Bathyancistrolepis trochoideus
Dall survive in the Okhotsk and Bering Seas as well as in the subarctic Pacific Ocean. Recent higher
water temperatures and a shallower sill depth may prevent the above three species from migrating backinto the Japan Sea.
Key words: Taxonomy, distribution, Ancistrolepidinae, Pliocene, Pleistocene
Introduction

Parancistrolepis (type genus of the subfamily Parancistrole-

The buccinid subfamily Ancistrolepidinae is a group of
cold-water species now living mainly off Hokkaido and in the
Okhotsk and Bering Seas. Unlike Neptunea, Buccinum andother buccinids, this group did not invade the Arctic andNorth Atlantic basins after the opening of the Bering Strait
during Pliocene time (Titova, 1993). This subfamily wasestablished by Habe and Sato (1972) as Ancistrolepisinae,
based on characteristics of the radula. When Goryachev(1987) revised the so-called Buccinidae, he correctly used
the subfamily name of Ancistrolepidinae.
According to Habe and Sato (1972), this subfamily consistsof the following five genera: Ancistrolepis Oall, Clinopegma
Grant and Gale, Neancistrolepis Habe and Sato, Bathyancistrolepis Habe and Ito and Pseudoliomesus Habe and Sato.
Thereafter, Tiba and Kosuge (1982) considered Bathyancistrolepis as a subgenus of Ancistrolepis, and stated that thetype species of Neancistrolepis should be included in thegenus Clinopegma. When Kantor (1988) studied the shellmorphology and radula. of Clinopegma, he considered it asubgenus of Ancistrolepis. Moreover, Goryachev (1987)
added Sulcosisus Oall and Japelion Oall to this subfamily.
Recently, Egorov and Barsukov (1994) included the genus

pidinae) in the Ancistrolepidinae. However, they did notindicate the reason why Sulcosinus, Japelion and Parancistrolepis should be included in the Ancistrolepidinae. In thispaper, we follow Habe and Sato's concept of the subfamily.
When Gladenkov et al. (1988) summarized the taxonomy of
buccinids from the Neogene of Kamchatka, they discriminated the Ancistrolepis grammatus group from the type A.
eucosmius group on the basis of large shell size and prominent T -shaped cords as independently noticed by Naruse(1952). Gladenkov et al. (1988) considered that the grammatus group belongs to the genus Neancistrolepis Habe andSato (1972). However, the type species of Neancistrolepis,
N. beringiana (Oall), differs from the grammatus group in its
rather obsolete spiral ribs.
Thereafter, Titova (1993) regarded the grammatus group as
belonging within Ancistrolepis and discussed the early evolution of the Ancistrolepidinae. According to her, this group
includes the following Recent species: Ancistrolepis grammatus (Oall), A. hikidai Kuroda, and A. kawamurai Habe andIto. On the other hand, the Ancistrolepis eucosmius group
has a small ovate shell and includes some Recent eastern
North Pacific species such as A. eucosmius (Oall), A. californicus Oall, and others. She also suggested that the eucos-

468

Kazutaka Amano et a/.

mius and grammatus groups evolved independently andmost genera of Ancistrolepidinae originated in cold-water
environments. However, Plio-Pleistocene fossils were notsufficiently considered by her.
Up to this time, the following species and subspecies ofAncistrolepidinae have been described from Plio-Pleistocene strata of Japan: Ancistrolepis masudaensis Nomura,A. peulepis Kanehara, A. koyamai (Kuroda), A. eucosmius
koyamai Habe and Ito, Bathyancistrolepis trochoideus Dall,
B. t. tokoyodaensis Ozaki, Clinopegma fragi/is Kuroda, C.
borealis Tiba and C. unicum (Pilsbry) (Kuroda, 1931 ; Suzuki,
1935; Nomura, 1937; Kanehara, 1937; Ozaki, 1958; Noda,
1962; Noda et a/., 1984; Amano, 1984; Noda and Amano,

1985; Matsui, 1985; Baba, 1990; Matsuura, 1992). The
first four species belong to the Ancistrolepis eucosmius
group (Gladenkov et a/., 1988). In the Plio-Pleistocene, no
species of the A. grammatus group has been recorded.
With the exception of Bathyancistrolepis trochoideus, eachspecies of Ancistrolepidinae occur only at one or a few
localities.
Fortunately, we collected some specimens of the Ancistrolepis grammatus group from Plio-Pleistocene strata in
Honshu and Hokkaido. Moreover, A. masudaensis andClinopegma borealis were found from new localities in
Honshu. In this paper, after describing these specimens, we
discuss their distribution and biogeographic significance.

140'

Japan Sea

40' ------&-------\.------

Pacific Ocean

Figure 1. New localities of Plio-Pleistocene Ancistrolepidinae (using the topographical maps "Furaoi" "Iwakisan", "Echigoshimoseki", "Ugosakai" and "Kanazawa", scale 1 : 25,000 published by Geographical Survey I~stituteof Japan).
Figure 2. 1-6. Ancistrolepis masudaensis Nomura, 1a-b, 3a-b: JUE nos. 15565-1, -2, Loc. 3, Tentokuji Formation, x1.7,
2a-b: JUE no. 15566-1, :,<2, 6a-~: JUE no. 15566-2, X1.5, Loc. Roadside cliff at Shohei Bridge near Masuda, Akumi County,
Yamagata Pref., Kannonjl Formation, 4a-b: Loc. Kakuma, Kanazawa City, Ishikawa Pref., Omma Formation, collected by Dr.
N: Mat.suura,. X1.5, 5a-b: SHM no. 12636, Holotype, X 1.7. 7,10. Ancistrolepis koyamai (Kuroda), 7: JUE no. 15567, Loc.
RI~erslde cliff nea~ O~ata, Nakajo village, Nagono Pref., Joshita Formation, X1.2, 10: JC 610067, Holotype, X1. 8,9.
Clmopegma borealis Tlba, 8a-c: 8a, x1.5,8b-c, X1, JUE no. 15568-1,9: JUE no. 15568-2; Lon. 4., Kuwae Formation, x1.
11a-b. Ancistrolepis peulepis Kanehara, IGUT 10988, Loc.84-01 of Noda and Amano (1985), Yuchi Formation X1.5. 12a-b.
Ancistrolepis aff. hikidai Kuroda, JUE no. 15569, Loc.2, Higashimeya Formation, X 0.8.
'

1013. Plio- Pleistocene Ancistrolepidinae of Japan

469

Kazutaka Amano et al.

470
New localities of Ancistrolepidinae

Five species were newly collected from the following five
localiteis (Figure 1). These localities, with stratigraphical andfacies details, are described below.
Loc. 1. Large roadside cliff about 850 m east of the passbetween Kitaubushi and Kitakawaguchi, Teshio town,
northwestern Hokkaido (fossil locality of Noda et al., 1983) ;siltstone bearing many calcareous concretions; lower partof Yuchi Formation.
Loc.2. Riverside cliff about 3.2 km upstream of Taiaki River
from its junction with the Iwaki River, Hirosaki City, Aomori
Pref.; siltstone; Higashimeya Formation.
Loc.3. Large riverside cliff along Yodo River, about 500 m
southwest of Awasegai, Kyowa town, Akita Pref. (Loc. T8of Ogasawara et al., 1986); pebble-bearing fine-grainedsandstone; Tentokuji Formation.
Loc. 4. Riverside cliff of small creek of Onnagawa River,about 600 m south of Housaka Bridge, Sekikawa village,
Niigata Pref.; siltstone; Kuwae Formation.
Loc. 5. River bank 260 m downstream of Sai River from theMegane Bridge, Kanazawa City, Ishikawa Pref. (sixth
sedimentary cycle of Omma Formation by Kitamura andKondo, 1990); fine-grained sandstone; middle part ofOm rna Formation.

Taxonomy
Family Buccinidae Rafinesque, 1815
Subfamily Ancistrolepidinae Habe and Sato, 1972
Genus Ancistro/epis Dall, 1895

Ancistro/epis masudaensis Nomura, 1937
Figures 2-1-6
Ancistrolepis masudaensis Nomura, 1937, p.177, pI. 24, figs.14a,b.
Ancistro/epis eucosmius koyamai Habe and Ito. Matsuura, 1992,

pI. 5-15 (2), fig. 4.

Type Specimen.-Holotype, SHM no. 12636 (Figures 2-5a-b).
Type Ioca/ity.-Masuda, Akumi County, Yamagata Pref.
Materia/.- Three specimens collected from Loc.3 (lower
Pliocene Tentokuji Formation).
Description.-Shell small, ovate-fusiform, solid, with low
spire. Whorls six, with two small and smooth protoconch
whorls. Penultimate whorl ornamented with three to four
rounded spiral ribs, separated by nearly equal interspaces.
Body whorl sculptured by seven to eight spiral cords, separated by slightly narrower interspaces. Subsutural ribs
distinct, just below well marked suture. Whole surface
occasionally covered by distinct growth lines. Aperture
ovate, nearly equal in length to spire. Inner side of outer lip
crenulated in correspondence with spiral ribs. Adapicalchannel narrow and deep. Inner lip with rather thick callus.
Canal short, recurved, forming rather distinct fasciole.

Measurements (in mm).NSP**
NSB*
DiameterSpecimens
Height48
11.2
JUE no. 15565-1 19.0
37
11.2
JUE no.15565-2 19.1
* Number of spiral cords on body whorl, * * Number ofspiral cords on penultimate whorl
Remarks.-Only a single specimen was described by
Nomura (1937) from the Plio-Pleistocene Kannonji Formation.
Morphological examination of the holotype (Figures 2-5a-b)
and two specimens (Figures 2-2a-b, 6a-b) which we collected from the same formation near Masuda shows thatAncistrolepis masudaensis is characterized by a small,ovate-fusiform shell, with low spire, 7-8 spiral cords on the
body whorl and 3-4 spiral cords on the penultimate whorl.
As described above, all these characteristics are the same in
the Tentokuji specimens.
Matsuura (1992) illustrated a single specimen (Figures 24a-b) from the Omma Formation at Kakuma, Ishikawa
Prefecture under the name of Ancistrolepis eucosmius
koyamai Habe and Ito [non A. koyamai (Kuroda)]. The
specimen has two protoconch whorls, a low spire, nine spiralcords on the body whorl and three spiral cords on the
penultimate whorl. These traits are shared with Ancistrolepis masudaensis. A. eucosmius koyamai is characterized byhaving a high spire and minute interstitial threads which arenever seen in A. masudaensis.
Comparisons.- The present species resembles Ancistrolepis koyamai (Kuroda), A. peulepis Kanehara, A. kamtchaticus(llyina) and A. eucosmius (Dall).
Ancistrolepis koyamai (Figures 2-7, 10) was originally described from the Pliocene Takafu Formation in northern
Nagano Prefecture under the generic name of Buccinum by
Kuroda (1931). It resembles A. masudaensis in shell shape,size and similar number of spiral cords (eight on body whorl
and three on penultimate). However, A. koyamai has rather
a flat area just below the suture and broader spiral cords
than A. masudaensis. Ancistrolepis peulepis (Figures 2-11ab) was proposed from the Pliocene Yuchi Formation innorthwestern Hokkaido by Kanehara (1937). This species
can be distinguished from A. masudaensis by its larger shell,
six broad spiral cords on the body whorl and by having a flatbottomed groove just below the suture.
Ancistrolepis kamtschaticus was established by lIyina(1939) under the name Buccinum strigillatum Dall var. kamtschatica from the Middle Miocene Kavran Suite (= Etolon
Suite). This species is allied to A. masudaensis and A.
peulepis in its shell form and in having four spiral cords on
the penultimate whorl. According to Gladenkov et al. (1988),
A. kamtschaticus has more numerous spiral ribs (8-10) on the
body whorl than the later two species.
The Recent species Ancistrolepis eucosmius (Dall) can beeasily distinguished from A. masudaensis by having many
interstitial spiral threads over the whole surface.
Distribution.-Pliocene Tentokuji Formation; Plio-Pleistocene Kannonji Formation; lower Pleistocene Om rna Formation, all in Honshu.

1013.

Plio- Pleistocene Ancistrolepidinae of Japan

Ancistrolepis grammatus (Oall, 1907)
Figures 3- 2- 4
(Ancistrolepis) grammatus Oall, 1907, p. 158 ;Kosuge, 1972, pI. 17, fig. 8.
Ancistrolepis grammatus (Oall). Oall, 1925, p. 3, pI. 30, fig. 8 ;Kuroda, 1931, fig. 6 ; Shikama, 1957, p.35, pI. 10, figs. 8a- b ;Habe and Ito, 1968, p. 3, 6- 7, pI. 1, fig. 1 ; Tiba and Kosuge,
1981, p. 5, 6 ; Okutani et al., 1988, p. 107 ; Bogdanov andSirenko, 1993, p. 52, pI. 52, figs. 1, 2.
Ancistrolepis grammatus yamasakii Kuroda, 1944, p. 237- 238, pI.
7, fig. 1; Habe and Ito, 1965, p. 56- 57, pI. 16, fig. 8.
Ancistrolepis grammata grammata (Oall). Habe and Ito, 1965, p. 57,
text- fig. 23.
Ancistrolepis grammata (Oall). Habe and Sato, 1972, pI. 1, fig. 8.
Ancistrolepis (Ancistrolepis) grammatus grammatus (Oall) Egorov and Barsukov, 1994, p. 6, fig. 16H.
Ancistrolepis (Ancistrolepis) grammatus yamazakii Kuroda, Egorov
and Barsukov, 1994, p. 7, figs. 31, 16E- G.

47 1

but strong cords. Subsutural groove narrow and rather
deep. Inner lip with thin callus. Fasciole not so large andsmooth.

Chrysodomus

Type specimen .-Holotype, USNM no. 110472.
Type loca/ity.-Tsugaru Strait (300 fms.).
Materia/s.-Two imperfect specimens obtained from Lac. 5(lower Pleistocene Omma Formation).
Description.- Shell medium- sized, thin, with more than fivesubtabulated whorls. Protoconch large, with two whorls.
Surface of each spire whorl covered by six prominent Tshaped cords. Body whorl sculptured by eleven weathered

Measurements (in mm).Specimens
Height~iameter
NSB *
NSP**
JUE no. 15571
6
JUE no. 15572
55.9 +
32.9 +
11
6* Number of spiral cords on body whorl, * * Number ofspiral cords on each whorl except for the lastRemarks .-Our specimens can be identified with therecent species Ancistrolepis grammatus (Oall) especially by
the form and number (5- 6 on penultimate, 8- 13 on bodywhorl in modern form) of spiral cords. They slightly differ
from some typical specimens of the species in having alower spire and narrower interspaces between cords. The
Recent species shows wide variations in spire height, and in
number and shape of the spiral cords (Tiba and Kosuge,1981). Therefore, the Omma Formation specimens fall within
the shape range of the Recent speCies.
Ancistrolepis grammatus yamasakii was discriminated fromthe typical grammatus by Kuroda (1944) because of its
narrower and more numerous (13) spiral cords. Tiba andKosuge (1981 , p. 8) treated this subspecies as a variety of A.
grammatus. As A. grammatus shows a wide range of varia-

Figure 3. 1. Ancistrolepis sp., JUE no. 15570, Loc. 1, Yuchi Formation, x 1. 2- 4. Ancistrolepis grammatus(Oall), 2a: x 1.5, 2b : x 1.55, JUE no. 15571, 3a- b : JUE no. 15572, Loc. 5, Omma Formation, x 1, 4 : JUE no. 15573,
Loc. off Rausu, Hokkaido, Recent, x 1.

Kazutaka Amano et al.

472tion in its shell shape, form and number of spiral cords, we
agree with Tiba and Kosuge's opinion.
Comparisons.-Ancistrolepis hikidai Kuroda differs from A.
grammatus in having more numerous spiral cords (8 onpenultimate and 13-15 on body whorl) and a larger bodywhorl.
Distribution.-Lower Pleistocene Omma Formation in
Honshu; Recent Tsugaru Strait (300 fms.), off Rausu and off
Abashiri in Hokkaido; Paramushir and Shumsh Islands (Kurile Islands).

Ancistrolepis sp. aff. A. hikidai Kuroda, 1944
Figures 2-12a-b
Material.-One imperfect specimen collected from Loc.2(upper Pliocene Higashimeya Formation).
Description.-Shell large, thick, with more than four
subtabulated whorls. Protoconch absent. Height of bodywhorl about three-fifths of shell height. Subsutural area
narrow and deep. Surface of penultimate whorl ornamented with ten quadrate or rounded spiral cords and one weak
rib just below subsutural keel. Body whorl with more thantwelve quadrate spiral cords and two rounded interstitial ribs.
Spiral cords on body whorl subdivided into two or three partsby shallow grooves. These cords on both whorls broader
than interspaces. Aperture partly broken.
Measurements (in mm).Specimens
HeightDiameter
JUE no. 15569 106.9+
64.3+- Number of spiral cords on body whorl,cords on penultimate whorl

NSP-*
NSB*
10
12+
'-Number of spiral

Remarks and comparisons.-The present specimen partly
resembles the Recent species, Ancistrolepis hikidai Kuroda(occasionally misspelled as A. hikitat) in having a similar
number of spiral cords. However, the following characters
are never seen in the Recent form; rather high spire, someinterstitial ribs and shallow grooves on spiral cords. The first
two traits can be seen in A. vietnamensis Sirenko andGoryachev (1990). The number of spiral cords enables us toseparate ~. vietnamensis (5 on penultimate and 20 on bodywhorl) easily from the Higashimeya specimen.

Ancistrolepis sp.
Figure 3-1
Material.-One poorly preserved specimen collected from
Loc.1 (lower Pliocene Yuchi Formation).
Description.-Shell large, thin, with more than four whorls'
lacking protoconch whorls. Body whorl very large OCCUpy~
ing four-fifths of shell height. Subsutural area broad andflat. Surface of penultimate whorl sculptured by fiverounded spiral cords with interspaces broader than cords
themselves. Body whorl with ten highly rounded cords
separated by broad interspaces.

Measurements (in mm).NSP**
NSB*
DiameterSpecimens
Height51049.6+
JUE no. 15570
85.7 +- Number of spiral cords on body whorl, ** Number ofspiral cords on penultimate whorl
Remarks and comparisons.-Judging only from the numberof cords of this specimen, it is allied to a Recent species,
Ancistrolepis grammatus (Oall). However, the former differsfrom the latter in having a large body whorl, a broad and flat
subsutural area, and highly rounded spiral cords. Owing to
the poor preservation of this specimen, it is too difficult toassign the shell at the species level.

Genus Clinopegma Grant and Gale, 1931
Clinopegma borealis Tiba, 1969
Figures 2-8-9Clinopegma borealis Tiba, 1969, p.135-136, pI. 7, figs. 1-5; Tiba
and Kosuge, 1982, p. 11-12; Amano, 1984, p.104, figs. 2, 3;
Matsui, 1985, p.175, pI. 23, figs.8a-b.
Sulcosinus borealis (Tiba). Egorovand Barsukov, 1994, p. 20-21,
figs. 3N, 5J, 15, 28C.
Material.- Two specimens collected from Loc.4 (lower
Pliocene Kuwae Formation).
Description.-Shell medium in size, consisting of sevenwhorls including two large protoconch whorls. Spire rather
low. Each whorl with angulated shoulder providing narrowand flat subsutural area. Aperture ovate with nearly straight
inner lip. Surface smooth except for fine growth lines andweak spiral threads.
Measurements (in mm).Specimens
Height
JUE no. 15568-1
65.1

Diameter
36.6

Remarks.-Shells of Ancistrolepidinae generally show awide range in spire height as described above. In spite ofits slightly low spire, the present specimen can be safely
identified with a Recent boreal species, Clinopegma borealis
Tiba, because of its similar shell shape and ornamentation.
When they described the species, Egorov and Barsukov(1994) includes this species in the genus Sulcosinus Oall
without any explanation including detailed information aboutan operculum and soft body of Sulcosinus. The typespecies of Sulcosinus is characterized by a thick callus,
deeply channeled suture and conspicuous zigzag ornamentation. None of these traits is observable in borealis.
Therefore, it is better for borealis to be included in Clinopegma rather than in Sulcosinus.
Comparisons.- The present species is closely related to
Clinopegma orientalis (Golikov and Gulvin) from the northern
Kurile Islands. The latter species differs from the former
only in having more distinct ribs, especially on the bodywhorl.
Distribution.-Pliocene Rumoi Formation in Hokkaido
Sasaoka and Kuwae Formations in Honshu; Recent off
Kamchatka, Bering Sea.

1013.

Plio-Pleistocene Ancistrolepidinae of Japan

473

Distribution

pis grammatus has been recorded from off Abashiri, off

The following species of Ancistrolepidinae have beenrecognized from the Plio-Pleistocene in Japan: Ancistrolepis masudaensis Nomura, A. peulepis Kanehara, A. koyamai(Kuroda), A. grammatus (Dall), A. aff. hikidai Kuroda, A. sp.,
Bathyancistrolepis trochoideus Dall, Clinopegma borealis
Tiba, C. tragi/is Kuroda, and C. unicum (Pilsbry). Amongthese ten species, four species suffered extinction after the
Pleistocene: namely, A. masudaensis, A. peulepis, A.
koyamai and C. tragi/is. It is noteworthy that the A. eucosmius group shows a high extinction rate.
The extant species of Ancistrolepidinae now live in thelower sublittoral to upper bathyal zone (Table 1). Ancistrole-

Rausu and the Okhotsk Sea (Higo and Goto, 1993) (150-300
m depth after Higo and Goto, 1993; 400-800 m after
Okutani et a/., 1988; 88-890 m after Egorov and Barsukov,
1994). Clinopegma borealis is found living off Kamchatka
and the Bering Sea (Higo and Goto, 1993) (100-300 m indepth after Higo and Goto, 1993). C. unicum has beenreported from off Kashimanada-Sanriku and southern Hokkaido (Tiba and Kosuge, 1982) (50-200 m in depth after Higoand Goto, 1993; 50-450 m after Okutani et a/., 1988) andfrom the southern part of the Okhotsk Sea and Sakhalin(Egorov and Bersukov, 1994) (100-250 m after Egorov andBarsukov,1994). In contrast with the above boreal species,
Bathyancistrolepis trochoideus occurs on the Pacific side ofeAncistroJepis masudaensis Nomura
OA. koyamai (Kuroda)eA. peuJepis Kanehara+A. grammatus (Da11)<)A. aff. bikidai Kuroda¢A. sp .
• BatbyancistroJepis trocboideus (Da11)
JJ..Clinopegma borealis Tiba
.6 C. unicum (Pilsbry)
A C. fragilis (Kuroda)

0030o--------~~------------------~----------------

Figure 4.

Distribution of Ancistrolepidinae from Plio-Pleistocene strata in Japan.

Kazutaka Amano et a/.

474
Table 1.

Distribution of some Recent species of Ancistrolepidinae occurring from Plio-Pleistocene strata in Japan.

Species
Ancistrolepis grammatus
Clinopegma borealis
C. unicum

Geographical distribution
off Abashiri off Rausu and Okhotsk Seal)
off Kamch~tka and Bering Seal)
Kashimanada-Sanriku and Southern Hokkaido4 ):Southern part of Okhotsk Sea and Sakhalin 3)
Kumanonada, Sagami Bay and off Sanriku 4 )Bathymetric range
150 300 ml ): 400 800m 2): 88 890 m3 )100-300 ml )50-200 ml ): 50-450 2 )100-250 m3 )100-1,500 ml ): 200-2,000 m2 ):620-2,050 m3 )Bathyancistrolepis
trochoideus
1) Higo and Goto (1993), 2) Okutani et al. (1988), 3) Egorov and Barsukov (1994), 4) Tiba and Kosuge (1982)

Honshu; Kumanonada, Sagami Bay, Kashimanada and off
Sanriku (Tiba and Kosuge, 1982) (100-1,500 m in depth after
Higo and Goto, 1993; 200-2,000 m after Okutani et a/.,1988; 620-2,050 m after Egorov and Barsukov, 1994).
As shown in Figure 4, all the fossil species occur only in
the Japan Sea borderland except for Bathyancistrolepis
trochoideus and Clinopegma unicum. It is significant tonote that all the species still extant from Plio-Pleistocene
strata on the Japan Sea side of Honshu such as Ancistrolepis grammatus, B. trochoideus and C. borealis are not foundin the Recent Japan Sea. Moreover, the Pliocene localities
from which C. borealis has been obtained are north of thosefor B. trochoideus. This occurrence is similar to the present-day distributional pattern; as noted before, C. borealis is
now found living off Kamchatka and the Bering Sea while
Bathyancistrolepis trochoideus occurs more southerly.
Biogeographic significanceIn the Pliocene and early Pleistocene, cold-water species
dominated the molluscan faunas of the Japan Sea borderland (Ogasawara, 1994; Amano, 1994). Therefore, someboreal populations of Ancistrolepidinae were able to invade
the Japan Sea through a northern channel (Tada, 1994)
which was more deeper than the modern water passways.
Later, especially during late Pleistocene glacial lowstands,
the Japan Sea was enclosed and its deep-sea bottom waseuxinic (Tada, 1994). Matoba (1978,1984) has pointed outthat the deep-water benthic foraminiferal fauna suffereddrastic extinction during the late Pleistocene. As mostlaNae of buccinid species including Ancistrolepidinae show
nonplanktotrophic development (Amio, 1963; Bouchet andWaren, 1994), their ability to disperse is less than that ofplanktotrophic laNae (Shuto, 1974). In the deteriorated
environments of cold-climate maxima, most species ofAncistrolepidinae in the Japan Sea borderland suffered
extinction along with the benthic foraminifers. However,Bathyancistrolepis trochoideus sUNived because it also
occurred on the Pacific side. Ancistrolepis grammatus andClinopegma borealis probably sUNived in the Okhotsk andBering Seas. However, unfortunately, this speculation is notsupported by the fossil record from the Plio-Pleistocene in
Sakhalin and Kamchatka, perhaps because the species arerare.
In the Holocene, with the Tsushima warm current flowing
over the hyperoxic bottom water, water temperature at thenorthern shallow straits increased over that in Plio-Pleis-

tocene times (see Amano,1994). Therefore, boreal Ancistrolepis grammatus and Clinopegma borealis could notinvade the Japan Sea. Why can not Bathyancistrolepis
trochoideus living on the Pacific side of Honshu migrate into
the Japan Sea?
Fossil occurrences of two species of Neptunea are shownin Figure 5. The genus Neptunea in phylogenetically close
to the genus Ancistorolepis (Titova, 1993). Among the
Recent Japanese Neptunea species, N. (Neptunea) intersculpta (Sowerby) and N. (Barbitonia) arthritica (Bernardi) havebeen recorded from the Plio-Pleistocene on both the Pacific
Ocean side and the Japan Sea side of Northeast Honshu aswell as the Japan Sea side of Hokkaido (Masuda and Noda,
1976; Nemoto and O'hara, 1979; Baba, 1990). Bothspecies are now living around the Japanese Islands. N.
intersculpta occurs in the Japan Sea and also off Sanriku,
Sakhalin and the Kurile Islands (Tiba and Kosuge, 1988) (36895 m in depth after Golikov, 1963). N. arthritica is known
from the Japan Sea, Okhotsk Sea and Pacific Ocean side ofNortheast Honshu (Tiba and Kosuge, 1988) (0-150 m in depth
after Golikov, 1963). These cool-water species can live inshallow waters. This enabled both species of Neptunea togo through the Recent northern straits into the Japan Sea.
In contrast, because the shallowest depth occurrence ofBathyancistrolepis trochoideus is still deeper than that ofthese Neptunea species, the former cannot invade the
Recent Japan Sea.
The distribution of Ancistrolepidinae in the Plio-Pleistocene and the Recent reveals that most deep-water elements in the Japan Sea suffered extinction during the
Quaternary. Thermal tolerance and bathymetric distribution
dictated which species could re-invade the Japan Sea after
these extinction events. Moreover, one of the reasons why
this group could not invade the Arctic and North Atlanticbasins with the Pliocene Beringian transgression is due totheir having deeper habitats than Neptunea, Buccinum andso on.
Acknowledgments
We are grateful to Prof. Geerat J. Vermeij of the Universityof California at Davis, and Prof. Takashi Okutani of Nihon
University for their critical reading of the manuscript. Dr.
Ludomila V. Titova of Moscow State University and Dr. Boris
I. Sirenko of Zoological Institute, Russian Academy of Sciences provided useful information on taxonomical problems.
We thank Prof. Hiroshi Noda of the University of Tsukuba, Dr.

1013.

Plio-Pleistocene Ancistrolepidinae of Japan• Neptunea (Neptunea) intersculpta (Sowerby)... N. (Barbitonia) arthritica (Bernardi)

0030o----------~------------------------r_-------------------

Figure 5.

Distribution of two species of Neptunea from Plio-Pleistocene strata in Japan.

Nobuomi Matsuura of the Shiramine-mura Dinosaur
Museum, Dr. Sadako Takeuch of the Saito Ho-on Kai
Museum of Natural History, Mr. Teiji Sato of Murakami HighSchool, and Mr. Tetsuya Tanaka of Joetsu University of
Education for their help in examining some fossil specimens.

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KitaubushdtBE±, Yuchi :lJ3~, Taiaki ::kt'<, Higashimeya J!:!Ei§f, Awasegai .g.~, Tentokuji 7C~~, Housaka ;j:~:tlii, Kuwae jf);iI, Omma ::k~, Masuda fHE

Trans. Proc. Palaeont. Soc. Japan, N.S., No. 182, pp.478-483, 6 Figs., June 30, 1996
© by The Palaeontological Society of Japan 1996

\1014\ A new genus of shrew from the Pliocene of Yinan,
Shandong Province, northern China
CHANG-ZHU JIN and VOSHINARI KAWAMURA
Institute of Vertebrate Paleontology and Paleoanthropology, Academia Sinica, p.o. Box 643, Beijing, China
Department of Earth Sciences, Aichi University of Education, Kariya, Aichi Prefecture, 448 Japan

Received 26 November 1995; Revised manuscript accepted 26 February 1996

Abstract. A large shrew mandible with pigmented teeth obtained from the Pliocene cave sediments ofYinan is referred to a new species of a new genus in the subfamily Soricinae, which is named Lunanosorex
Iii. This species belongs to the tribe Beremendiini of the subfamily. Comparisons with large shrews withpigmented teeth such as Beremendia, Blarinoides and Shikamainosorex indicate that Lunanosorex isclearly distinct from all the shrews. In north China, Lunanosorex appeared probably in the middle
Pliocene as an indigenous genus, and seems to have been coexistent with Beremendia until it became
extinct around the end of the Pliocene.
Key words: New genus, new species, Lunanosorex, shrew, Pliocene, north China
Introduction
In 1971, Pliocene cave sediments containing a large
number of mammalian remains were found on the Qipanshan
Hill near Xingtunzhi (=western hill of Shuangquan) in Yinan
County (Figure 1). Of the remains, Kowa/skia (cricetid rodent)
and Ursus (bear) were subsequently studied (Zheng, 1984;
Li, 1993), while others have remained undescribed. We
therefore resumed systematic studies of these remains inorder to elucidate the mammalian fauna of this locality,
which was expected to provide important knowledge on the
Pliocene mammalian fauna of north China. In the course of
our study, we found that the remains contained an interesting large shrew mandible with pigmented teeth. This
mandible shows unique characters which allow it to bereferred to a new genus. In this paper, we describe themandible in detail, and discuss its systematic position.
Geological setting
The sediments completely infill a fissure-like cave which isformed in Ordovician limestone. The plan of the cave isobservable, because the ceiling of the cave has been
removed. In plan, the cave has a northeast-southwest
trend, and is about 15 m long and about 4.8 m in maximum
width. The sediments are strongly cemented by carbonates
into cemented breCCia, sandstone and mudstone. Renewed excavations conducted in October and November 1987
reveal the following sequence in descending order (thickness shown in parenthesis):
Layer 1 : Reddish brown breccia (110 cm)
Layer 2: Reddish brown breccia (87 cm)

Layer 3: Reddish brown muddy breccia (115 cm)
Layer 4: Reddish brown muddy breccia (140-170 cm)
Layer 5: Reddish brown muddy sandstone with breccia(50-100 cm)
Layer 6: Brown fine-grained sandstone with breccia (110120 cm)
Layer 7: Reddish brown fine-grained sandstone (140 cm)
Layer 8: Reddish brown calcareous mudstone with breccia (30cm)
Layer 9: Brown fine-grained sandstone (more than 30 cm)
The shrew mandible described below was obtained from
Layer 6.

Terminology and measuring method
The terminology and measuring method follow those of Jin
and Kawamura (1996). All the measurements have beentaken with a measurescope (Nikon: MM-11) with an electric
digital counter (Nikon: CM-65).

Systematic paleontology
Order Insectivora Bowdich, 1821
Family Soricidae Gray, 1821
Subfamily Soricinae Fischer von Waldheim, 1817
Tribe Beremendiini Reumer, 1984
Genus Lunanosorex gen. nov.
Type species.-Lunanosorex Iii sp. nov., described below.
Name derivation.-Named after Lunan, an area name,meaning the southern part of Shandong Province, plus sorex(Latin) meaning shrew.

1014.

New Pliocene shrew Lunanosorex from Yinan

Figure 1. Index map showing the location of the fossil
locality.

Diagnosis.-Large shrew with similarity to both Beremendia and Blarinoides; coronoid process longer and broader
than that of Beremendia; this process not leaning anteriorly,
but its apical part strongly protruding anteriorly; coronoid
spicule and external temporal fossa well developed; upper
pterygoid fossa indistinct; upper facet narrowly elliptical;
interarticular area very broad and having lingual emargination; lower facet placed very anteriorly, and thus invisible inbuccal view; internal temporal fossa deeply pocketed, andcontinuing to mandibular foramen through a small opening;dental formula 1-2-3 for lower teeth; teeth stained red todark red; antemolars and molars having thick cingulum; P4
with posterolingual basin; entoconid crest present in MI'
Included species.-Monospecific, including L. Iii only.
Geographic and geologic distribution.-Known only fromthe locality of Yinan; Late Pliocene.

Lunanosorex Iii sp. nov.
Figures 2-6
Holotype.-A left mandible with a first lower incisor, Alo P4
and MI to Ma (V10813), stored in the Institute of Vertebrate
Paleontology and Paleoanthropology, Academia Sinica.
Referred specimen.- The holotype only.
Locality and geologic age.-Qipanshan Hill near Xingtunzhi
in Yinan County, Shandong Province; Late Pliocene.
Name derivation.-Named in honor of Professor Li Chuankui, who has contributed to the studies on Cenozoic micromammals of China.
Diagnosis.-Same as for the genus.
Description.-The mandible is completely preserved
except for the apical part of the angular process. All theteeth are, however, strongly worn, considerably reducing theheight and pigmented area of the cusps and ridges.

479

Mandible: The horizontal ramus is stoutly built. It attains
its maximum height below Ma in buccal view, and below M2
in lingual view (Figure 2). The mental foramen is a small
opening in a shallow depression on the buccal face of theramus, and is situated below the hypoflexid of MI' Thesymphysis begins at the anterior tip of the ramus, andterminates below the posterior root of MI' It is formed by
two ridges and a deep groove between them. Of the tworidges, the upper one is more prominent. The groove opens
only posteriorly, because the ridges are confluent anteriorly.
The morphology of the ascending ramus is similar to that ofBlarinoides in general. The coronoid process is longer andbroader than that of Beremendia (Figure 3). This processleans greatly to the buccal side (Figure 4), but does not leananteriorly. The apical part of the process markedly
broadens in lateral and dorsal views owing to its remarkable
anterior protrusion (Figure 3; 1A and Figure 5). The tip of
the process is conspicuously thickened and forms a roundedsmooth surface with a small depression on its posterior part.
The coronoid spicule is very prominent, and extends diagonally on the buccal face of the coronoid process. The
areas above and below the spicule are strongly excavated toform the external temporal fossa. The upper sigmoid notchis high in position, and is relatively shorter than that ofBeremendia. It is somewhat emarginated ventrally (Figure
3; 18). There is no pterygoid spicule. The upper pterygoid
fossa is indistinct, and is much weaker than in Beremendia(Figure 3; 1C). The morphology of the condyle, however,resembles that of Beremendia (Figure 5; 2). The upper
facet exhibits a narrow transverse elliptic shape. The interarticular area with lingual emargination is very broad, anddiverges downward. Its buccal margin is rather straight.
The lower facet is formed on the ventral face of the lower
part of the condyle. In ventral view, its posterior margin isstrongly emarginated as in Beremendia (Figure 5; 2). The
lower part of the condyle greatly protrudes linguoventrally,
and is placed greatly anteriorly (Figure 3; 10), so that thelower facet cannot be seen from the buccal side (Figure 2A).
The internal temporal fossa with an oval outline is very large
and deeply pocketed. The mandibular foramen is large but
relatively shallow, and extends anteriorly. Its inner wall ispenetrated by a small opening which connects this foramenwith the internal temporal fossa (Figure 3; 1E). The lower
sigmoid notch is not remarkably emarginated as in Beremendia and Blarinoides. The lower pterygoid fossa forms abroad, shallow furrow extending from the mandibular foramen to the base of the angular process. A small boss isobserved below this furrow (Figures 28 and 3).
First lower incisor: The tooth projects straight forward in
dorsal view (Figure 6). Its apical part and cutting edge areconsiderably worn, so that their original shape cannot be
observed. The apical part is stained red to dark red. A
cingulum is observed along the buccal root-crown junction
line. This junction makes an acute buccal angle, andextends to a point somewhat posterior to the posterior
margin of P4 (in Beremendia, it is rounded and ends belowP4)' On the lingual face of the crown, there is neither
cingulum nor longitudinal groove, but a low ridge extending
from the tip of the crown to the junction line.

480

Chang-zhu Jin and Yoshinari Kawamura

Figure 2. Lunanosorex Iii gen. et sp. nov. Left mandible with the first lower incisor, AI, P, and MI to M3(holotype : V10813). A : buccal view, B : lingual view.

Al : This tooth is single-cusped, and overlies the first lower
incisor. The crown is rounded triangular in occlusal outline.
The apical part of the cusp is stained red. A small depression probably corresponding to the posterolingual basin of P4
is obseNed just behind the apex of the cusp. The buccal
face of the crown protrudes posteroventrallY' and has amarked thick cingulum. Another cingulum is present on the
lingual face, but it is quite indistinct.
P, : The anterior part of this tooth overlaps on the posterior
part of AI' The basic structure, pigmentation and occlusal
outline of the crown are roughly similar to those of AI ' The
central constriction of the occlusal surface suggests that two
cusps were originally positioned near to each other. The
posterolingual basin is well developed to form a broad valley
extending toward the posterolingual corner of the crown.

The posteroventral protrusion of the buccal face of thecrown is more developed than in AI, so that the buccal facelargely overhangs the mandible. A very thick cingulum
occurs on this face, while the cingulum on the lingual faceis thinner and less distinct.
MI and M2 : The occlusal outline is trapezoidal. The
ectolophid is stained red. The trigonid has nearly the same
width as the talonid. The protoconid is placed somewhat
anterior to the metaconid. The hypoflexid reaches the
buccal cingulum. A ridge extending anterolingually from the
hypoconid attaches to the posterior face of the protoconid.
Another ridge extending lingually from the hypoconid isseparated from the entoconid by a very narrow groove at theposterolingual corner of the crown. The entoconid crest ispresent in MI. In M 2 , however, it is unknown whether the1014.

481

New Pliocene shrew Lunanosorex from Yinan

2

o

2mm

~

Figure 3. Simplified sketch illustrating the mandibular ascending rami in lingual view, comparing Lunanosorex
Iii gen. et sp. nov. (1), Beremendia pohaiensis from Haimao (2), and the shrew mandible from the Yushe Basin (3).
1: V10813, (A: anterior protrusion of the apical part of the coronoid process, B: slight ventral emargination of theupper sigmOid notch, C: indistinct upper pterygoid fossa, D: anterior position of the lower part of the condyle, E:
small opening on the inner wall of the mandibular foramen), 2: DH8956, 3: V8895, 4.

~anteriorbual2

posterior

bual

o

2mm

L...-..J.......

Figure 5. Lunanosorex Iii gen. et sp. nov. Holotype(V10813). Simplified sketch illustrating the ascending ramus
in dorsal view (1) and the condyle in ventral view (2). Arrow
indicates the anterior protrusion of the apical part of thecoronoid process.

o

2mm.1.-_....1'

1-'_ _

Figure 4. Lunanosorex Iii gen. et sp. nov.
ascending ramus in posterior view (V10813).

Mandibular

crest is present or not owing to strong wear of the crown.
The straight buccal cingulum is very thick and distinct. On
the other hand, the lingual one is thinner, less distinct andslightly undulated.
Mg : The trigonid is preserved, while the talonid is mostly
absent, possibly due to wear. The protoconid is situatedslightly anterior to the metaconid. As in M, and M2 , thebuccal cingulum is thick and straight, while the lingual one
is indistinct and slightly undulated.
Measurement.-

Length from the mental foramen to the uppermost
point of the lower margin of the ascending
ramus ................................ 7.54 mm
Height of the coronoid process ............ 6.86 mm
Length of the upper facet.. .. .. .. .. .. .. .. .. 1.98 mm

Length from P4 to M2 .................... 5.83 mm
Length of the first lower incisor .. .. .. .. .. .. 5.86 mm
Length of Al ............................ 1.12 mm
Width of Al .............................. 1.00 mm
Length of P4 • • • • • • • • • • • • • • • • • • • • • • • • • • • • 1.83 mm
Width of P4 • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • 1.35 mm
Length of M, ............................ 2.67 mm
Trigonid width of M, ...................... 1.81 mm
Talonid width of M, ...................... 1.78 mm
Length of M2 ............................ 2.27 mm
Trigonid width of M2 ...................... 1.54 mm
Talonid width of M2 ...................... 1.49 mm
Trigonid width of Mg ...................... 0.98 mm
Systematic position.- This species has such characters as
the internal temporal fossa deeply pocketed, the interarticular area emarginated lingually, and P4 with posterolingual
basin, which are diagnostic of the subfamily Soricinae.
Reumer (1984) provided a revised key to subfamilies andtribes of the Soricidae in which he mainly followed theclassification by Repenning (1967), but added a new idea tothe tribal classification of the Soricinae. This key indicatesthat the present species belongs to his new tribe, Beremendiini, because it has a broad interarticular area of the482

Chang-zhu Jin and Yoshinari Kawamura

2mmoFigure 6. Left lower dentition of Lunanosorex Iii gen. et
sp. nov. Occlusal view of the dentition of the holotype(V10813).

condyle, and a lower facet strongly shifted anteriorly, as wellas pigmented teeth and the entoconid crest on M j • Reumer(1984) considered that the genus Beremendia is the only
constituent of the tribe. In comparion with the known
species of Beremendia (B. pohaiensis, B. fissidens and B.
minor; see Jin and Kawamura, 1996), the present species
differs in having a longer and broader coronoid process
whose apical part strongly protrudes anteriorly, stronger
coronoid spicule and external temporal fossa, and much
weaker upper pterygoid fossa (Figure 3). These differences
are considered to be sufficiently generic, because they are
greater than those among the species of Beremendia. The
present species is therefore referred to a second genus of
Beremendiini, Lunanosorex, which is newly recognized here.
Comparison and disGussion.-As already described in the
diagnosis, Lunanosorex is a large shrew with pigmented
teeth which shows similarity to both Beremendia and Bla-rinoides, but the differences from these genera are also
distinct. Those from Blarinoides are exclusively described
here, because those from Beremendia are mentioned above.
Blarinoides differs in having a distinct pterygoid spicule, anupper pterygoid fossa strongly excavated, lingual emargination of the interarticular area slighter, P4 with a uniquetetrahedral shape and without a posterolingual basin, and M j
without entoconid crest.
Two genera of large soricines with heavily pigmented
teeth have been hitherto described from East Asia. Theyare "Peisorex" from the middle Pliocene and early Pleistocene of north China and Shikamainosorex from the middle
and late Pleistocene of Japan. As already demonstrated by
Jin and Kawamura (1996), the former is synonymous with
Beremendia, and thus the same differences as thosementioned above are observed between "Peisorex" andLunanosorex.
On the basis of the description by Rzebik-Kowalska andHasegawa (1976) and the observation of comparative specimens (Y. Kawamura's collection), Shikamainosorex differsfrom Lunanosorex in having the tip of coronoid process not
protruding anteriorly, shorter upper facet, lower incisor extending more posteriorly, A j larger relative to P4, indistinct
buccal cingula of A j and P4 , M j with a thicker buccal
cingulum, and no entoconid crests in the lower molars.
The comparisons above indicate that Lunanosorex iseasily distinguishable from Blarinoides and Shikamainosorex
as well as from Beremendia. Lunanosorex is, however,similar to Blarinoides and Shikamainosorex in the generalmorphology of the ascending ramus, while it resembles
Beremendia in the shape of the mandibular condyle and thepresence of the entoconid crest in M j • More completematerials including upper dentition are necessary to elucidate its affinity to other soricine genera.
Additionally, a mandibular ascending ramus recently described from the middle Pliocene in the Yushe Basin (V8895,
4; fig. 1 of Flynn and Wu, 1994) is very similar to Lunanosorex
in having a long and broad coronoid process, strong coronoid
spicule and external temporal fossa, although this specimen
is somewhat smaller, the anterior protrusion of the apical partof its coronoid process is much weaker, and its upper
pterygoid fossa is better developed than in Lunanosorex(Figure 3). Flynn and Wu (1994) did not determine its taxonomic position, probably because it is fragmentary. In our
opinion, however, this specimen is possibly congeneric with
Lunanosorex, or even conspecific with L. Iii.
As regards the constituent genera of Beremendiini, Beremendia first appeared in the early Pliocene of Europe, but its
ancestor is unknown in Europe (Reumer, 1984). Somewhat
later in north China, Lunanosorex appeared, but its ancestor
is also unknown as far as the pre-Pliocene fossil records ofEast Asia are concerned. It probably coexisted with Beremendia in the late Pliocene of north China. Lunanosorex
seems to have become extinct before the beginning of the
Pleistocene, while Beremendia survived until the early Pleistocene there.

1014.

New Pliocene shrew Lunanosorex from Yinan

Museum of Natural History for encouraging us throughout
this study.

Conclusions
The large shrew mandible with pigmented teeth from the
Pliocene of Yinan is allocated to the tribe Beremendiini ofthe subfamily Soricinae. This tribe was previously considered to comprise only one genus, Beremendia. The mandible is referable to a new species of a new genus named
Lunanosorex Iii, because the differences between themandible and that of Beremendia are sufficiently generic.
Lunanosorex is, therefore, considered to be the second
genus of the tribe. In addition to the comparison with
Beremendia, it is compared with the large shrews, Blarinoides
and Shikamainosorex, known from the Pliocene of Europe
and the Pleistocene of Japan, respectively. Lunanosorex iseasily distinguishable from these two genera, and its relative
affinity to Beremendia is suggested. Lunanosorex inhabited
north China together with Beremendia in the later part of the
Pliocene, and possibly became extinct before the beginningof the Pleistocene.

Acknowledgments
We wish to express our thanks to Drs. Y. Tomida of the
National Science Museum (Tokyo) and L. J. Flynn of Harvard
University (Cambridge) for critical reading of this paper.
Thanks are also due to Associate Professor You Yu-zhu and
Mr. Li Yi-zheng of the Institute of Vertebrate Paleontology
and Paleoanthropology, Academia Sinica (Beijing) and Mr. Xu
Shu-bin of the Commission of Preservation of Ancient
Monuments of Linyi, Shandong Province for helping us in ourfield work. Finally, we would like to thank Professor H.
Kumai of Osaka City University and Mr. H. Taruno of Osakaw£li.

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i!f~T

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Transactions and Proceedings of the PalaeontologicalSociety of Japan
June 30, 1996

New Series No. 182
CONTENTS
TRANSACTIONS

1008. Hiroaki Karasawa: Shako, a new Miocene stomatopod Crustacea from Japan........ 413

1009. Shin'ichi Nishin?sono: Larval paleoecology of the late Pleistocene naticid gastropod
Cryptonatica with two protoconch types from the Oga Peninsula, northern Japan . . .. .. .. 419

1010. Chang - zhu Jin and Yoshinari Kawamura: The first reliable record of Beremendia(Insectivora, Mammalia) in East Asia and a revision of Peisorex Kowalski and Li, 1963 .. 432
1011.

Boo- keun Khim, Takami Nobuhara and David E. Krantz : Stable isotope records of the
Pliocene fossil Akebiconcha kawamurai (Bivalvia: Vesicomyidae) from the Tamari Formation, Central Japan : Indication of chemoautotrophic symbiosis .... ..... . .... . ...... ... 448

1012. Hiroshi Kitazato and Satoshi ry1atsushita: Laboratory observations of sexual and asexual
reproduction of Trochammina hadai Uchio . ........ ... ... .. ... .... " ... ..... . ... . ... '.. 454
1013. Kazu.taka Amano, Mikiko Ukita and Shinji Sato : Taxonomy and distribution of thesubfamily Ancistrolepidinae(Gastropoda: Buccinidae) from the Plio- Pleistocene ofJapan .. .. ... .• ... .. ... . .... .... . . . .. .. . .. ... . .... ...... . .... .. ...... .. ........... 467
1014. Chang - zhu Jin and Yoshinari Kawamura: A new genus of shrew from the Pliocene of
Yinan, Shandong Province, northern China ....... .. . . .. .... .. .. ... .... . .... .... ..... 478

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