Geobiology (2007), 5, 127–139

DOI: 10.1111/j.1472-4669.2007.00106.x

Methane-flux-dependent lateral faunal changes in a Late
Cretaceous chemosymbiotic assemblage from the Nakagawa
area of Hokkaido, JapanO R I G Ifaunal
LateralNA
L AchangesR T I CLtdLin
E a Late Cretaceous chemosymbiotic assemblage
Blackwell
Publishing

R OB E RT G . J E N KI N S 1 , 2 , A N D RZE J KA I M 1 , 3 , Y OSHINORI HIKID A 4 AND KAZUSHIG E TANABE 1
1Department of Earth and Planetary Science, University of Tokyo, Tokyo 113-0033, Japan
2

University Museum, University of Tokyo, Tokyo 113-0033, Japan
Institute of Paleobiology, Polish Academy of Sciences, ul. Twarda 51/55, PL-00-818 Warszawa, Poland
4Nakagawa Museum of Natural History, Hokkaido 068-0835, Japan
3

ABSTRACTA Late Cretaceous carbonate body (2 m in maximum diameter) surrounded by clastic rocks, recently discoveredin the Nakagawa area (Hokkaido, Japan), is interpreted as a methane-seep deposit, on the basis of negative
carbon isotopic composition (as low as −43.5‰), variable sulphide sulphur isotopic composition, high carbonate
content, and in situ fractures. It most likely formed owing to methane-bearing pore-water diffusion. We
estimate that the concentration of methane decreased toward the margin of the carbonate body, and that only
small carbonate concretions were precipitated at a certain distance from the methane-seep centre. These spatial
characteristics coincide well with the observed pattern of faunal distribution. The gastropod-dominated association (indeterminate abyssochrysids and ataphrids and the acmaeid limpet Serradonta sp. are most common)
co-occurs with lucinid and thyasirid bivalves ( Thyasira sp., Myrtea sp., and Miltha sp.), and was found within
and just above the methane-derived carbonate body. Acharax and Nucinella (solemyoid bivalves) are more
typical of the peripheral part of the methane-influenced sediments. We suggest that this pattern of faunal distribution reflects the decreasing concentration of methane and apparently also hydrogen sulphide when movingfrom the centre of discharge toward the periphery of the methane seep.
Received 13 April 2006; accepted 31 January 2007
Corresponding author: R. G. Jenkins; e-mail: robert@um.u-tokyo.ac.jp.

INTRODUCTION
The unexpected discovery of hydrothermal-vent and coldseep communities dependent on chemosynthetic bacteria for
their major energy sources (Lonsdale, 1977; Corliss et al., 1979;
Suess et al., 1985) stimulated large-scale investigation in all
the world’s oceans. Since the 1970s, such highly specialized
animals have been found at various sites where bottom water
is enriched with sulphide and methane supplied from hydrothermal
vents, cold-seeps, ground-water seeps, whale skeletal remains,
sunken driftwood, and even from rotting cargo of a sunken
ship (Marshall, 1988; Smith et al., 1989; Dando et al., 1992;
Tunnicliffe, 1992; Hasegawa, 1997; Sibuet & Olu, 1998; Van
Dover, 2000).
The methane discharging from a methane seep usuallyoriginates from the activity of methanogens and throughcarbonate reduction or acetate fermentation under anoxic
conditions. It can also be formed by the thermal decomposition© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltdof organic matter (Whiticar, 1999; Kotelnikova, 2002). The
methane migrating from its place of origin up to the seafloor undergoes both aerobic and anaerobic oxidation. The
oxidation of organic matter generally takes place owing toseveral oxidants in the marine water column, which penetratemethane-containing sediment (Aller, 2004). Sulphates are
utilized in the last phase of this process (Aller, 2004). For thisreason, methane oxidization from sulphates takes place firstin the base of the sulphate-reducing zone (Valentine, 2002).
Recently, it has been shown that the anaerobic oxidation of
methane (AOM) is mediated by consortia of anaerobic
methane-oxidizing archaea (ANME) and sulphate-reducing
bacteria (SRB; Orphan et al., 2002). When the methane
discharges into a well-oxidized environment, the aerobic
oxidation of the methane may also be mediated by methanotrophic bacteria (Aharon, 2000).
The AOM reaction leads to an increase in alkalinity, which
is favourable for the precipitation of carbonate minerals

127

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R. G. JENKINS et al.

(Michaelis et al., 2002; Peckmann & Thiel, 2004). Suchmethane-derived carbonates are relatively easily recognizable
in the geological record, because they have a highly 13C-depleted
carbon isotopic signal and contain biomarkers that originated
due to the activity of methane-related micro-organisms(Peckmann & Thiel, 2004; Birgel et al., 2006a,b).
The macro-organisms in communities having diffusive or
effusive activity (i.e., hot vents and cold/methane seeps) are
faced with the serious problem of how to survive in anenvironment with a high content of toxic hydrogen sulphide(usually from a few to 25 mM in Recent methane seeps; Stakes
et al., 1999; Sahling et al., 2002; Levin, 2005), and how to
supply this compound to their intracellular symbionts(Childress et al., 1991). The differences in the ability ofparticular organisms to cope with these problems influence thepattern of faunal distribution. Sahling et al. (2002) reported
for Hydrade Ridge, in the Cascadia margin off Oregon, thatsulphur-oxidizing bacteria (Beggiatoa), vesicomyid bivalves(Calyptogena), and solemyid bivalves (Acharax) are distributed
according to a gradient in hydrogen sulphide concentration.
Beggiatoa occurs in the proximity of methane discharges withthe highest sulphide concentration, whereas Calyptogena
surrounds the bacterial mat, and Acharax occupies the peripheryof the seep (fig. 2 in Sahling et al., 2002). A similar pattern
has also been reported for other modern methane seeps(MacDonald et al., 1989; Barry et al., 1997; Olu et al., 1997;
Rathburn et al., 2003; Levin et al., 2003; Orphan et al., 2004).
Although faunal distribution in modern chemosynthesis-based
communities evidently is mainly controlled by hydrogensulphide concentrations (Barry et al., 1997; Sahling et al., 2002;
Knittel et al., 2005; Levin, 2005), other factors, including
depth and organism-generated microhabitats, may also be
relevant (Sahling et al., 2003; Bergquist et al., 2003; Levin,2005).
Several researchers have described the distribution patternof fossils within and/or around ancient methane-seep
deposits (Gaillard et al., 1992; Beauchamp & Savard, 1992;
Kauffman et al., 1996; Kelly et al., 2000; Campbell et al.,
2002; Peckmann et al., 2002; Campbell, 2006). However, few
workers have analysed both lithological and geochemical data
to decipher the relationship between the lateral distribution offossils and the spatial zonation of ancient methane-bearing
pore fluids.
The fossil record of chemosynthesis-based communities
suggests that they experienced a major faunal turnover during
the Mesozoic, particularly in the Late Jurassic to Late
Cretaceous (Campbell & Bottjer, 1995; Little & Vrijenhoek,
2003; Kiel & Little, 2006). Many modern benthic invertebrategroups entered vent/seep habitats in this time interval. Recent
molecular analyses of dominant vent and seep taxa suggest thatthey likely diversified during the past 100 Myr, in the Cretaceousand early Cainozoic (Black et al., 1997; Van Dover et al.,
2002; Little & Vrijenhoek, 2003). Thus, the Cretaceous wasa crucial period in the origin and evolution of modern vent andseep taxa. A precondition for clarifying the evolution ofchemosynthesis-based communities is deciphering the spatialdistribution pattern of taxa at Cretaceous methane-seep sites.
A great number of fossil and modern chemosynthetic
communities occur in the Japanese islands (Majima et al., 2005).
One of the best-preserved Late Cretaceous chemosynthetic
communities is in the Omagari Formation, Upper Yezo Groupat the Omagari site, in the Nakagawa area of northern
Hokkaido (Hikida et al., 2003). Hikida et al. (2003) inferred
the presence of a fossil chemosynthetic community associatedwith a methane seep at this site, based on carbon isotopic
composition, petrographical features, and a fauna of tube
worms, lucinid bivalves, tiny gastropods and brachiopods.
Regrettably, the carbonate body with this association is locatedon an isolated islet in the Abeshinai River. At present, it is
not possible to examine the entire sequence with its lateralvariations, or the boundary between the carbonate body andsurrounding siliciclastic sediments. During our field studies in
the Nakagawa area, we discovered additional carbonate bodies
in the Omagari Formation. We inferred that these bodies formed
due to methane-seep activity but, in contrast to the Omagari
site, their relationship to the host sediments is exposed well.
In this study we focus on a newly discovered locality at
Yasukawa and analyse the mode of occurrence, synsedimentary structures, and carbon and oxygen isotope ratios ofmethane-derived carbonates, along with the sulphur isotopic
composition of pyrite. Our objective is to trace spatial physicochemical changes in the Cretaceous methane seep and to learn
their importance for the distribution of the chemosynthesisdependent assemblage.

GEOLOGICAL SETTING
A thick marine-clastic sequence was deposited in the Yezo
fore-arc basin along the western margin of a subduction zone
in the circum-northwestern Pacific during the Cretaceous(post-Aptian; Takashima et al., 2004). This sequence is widelydistributed along more than 1000 km from northern Sakhalin
to southern Hokkaido (Matsumoto, 1942; Shigeta & Maeda,
2005). Takahashi et al. (2003) divided post-Aptian Cretaceous
deposits in the Nakagawa area into the Lower Yezo, Middle
Yezo, Upper Yezo, and Hakobuchi Groups, in ascending order(Fig. 2). The Upper Yezo Group in this area is subdivided into
the Nishichirashinai, Omagari, and Osoushinai Formations, inascending order (Fig. 2; Takahashi et al., 2003). The methaneinfluenced carbonate bodies discussed in this study developed
during sedimentation of the Omagari Formation (Fig. 2). The
largest known methane-seep-related carbonate body in the
Nakagawa area, reported by Hikida et al. (2003) at the Omagari
site, crops out near the junction between the Abeshinai Riverand the Osoushinai Creek (Fig. 1A). The carbonate bodies at
the Yasukawa site are located about 3 km downstream fromthe Omagari site (1 km downstream from the juncture with
Tannosawa Creek; Fig. 1A). Carbonate bodies at this site are© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Lateral faunal changes in a Late Cretaceous chemosymbiotic assemblage

129

Fig. 1 Sketch maps of Hokkaido and the Nakagawa area showing Yasukawa (44°40′37′′N, 142°1′27′′E) and Omagari (44°39′26′′N, 144°2′25′′E). (A) Geologicalmap of the middle reach of the Abeshinai River. Modified after Takahashi et al. (2003, fig. 1). (B) Geological sketch of the Yasukawa site (plan view). Four in situ
carbonate bodies, A–D, are exposed in the top sequence of the Omagari Formation; alt, alternating beds of sandstone and mudstone; ss, sandstone; ms, mudstone.

emplaced within sediments in the upper part of the Omagari
Formation, and have been dated as Lower Campanian basedon the first occurrence of Inoceramus (Platyceramus) japonicus(Takahashi et al., 2003). The Omagari Formation is characterizedby alternating greenish sandstone and sandy siltstone, with
common intercalations of pebble- to boulder-size gravel beds.
These sandstone beds include rip-up clasts in places, andexhibit incomplete Bouma sequences interpreted as turbidites.
Based on their poorly sorted texture and matrix-supported
structure, the gravel beds are interpreted as debris-flows. Theintercalated mudstone is poorly sorted, and typically contains
very coarse sand grains and granules. In addition, there aresyndepositional and early post-depositional structures consistingof slumping folds. These lithological features and sedimentary
structures suggest that the Omagari Formation was depositedat the interface between a continental-shelf margin and acontinental slope.

MATERIAL AND METHODS
Detailed observations were made of the mode of occurrence,and the lithological and palaeontological properties, of the© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

largest carbonate body at the Yasukawa site [carbonate body A(CBA), Fig. 1B], as well as the distribution patterns of small
concretions around it. We also examined the sedimentologicalfeatures of surrounding clastics at a locality 5 m northeast from
CBA [Yasukawa peripheral site (YPS), Fig. 1B]. Representativerock samples and macrofossils were collected from various
portions of the carbonate body and its enclosing strata.
Taxonomic identification was made whenever possible. Small(<10 mm) fossils were coated with platinum-palladium using
an ion coater, and studied using Hitachi S-2400S and Philips
XL20 scanning electron microscopes at the Department ofEarth and Planetary Science, the University of Tokyo (EPUT),
and the Institute of Paleobiology, Polish Academy of Sciences(ZPAL), respectively. The carbonate rock and concretion
samples were cut normal to the bedding plane and polishedby a graded series of carborundum powders, and finally by
0.25 µm diamond powder. Thin-sections were prepared,
upon which standard observations were performed by planeand cross-polarized and reflected light microscopy. X-ray diffraction analysis (XRD) was carried out on un-oriented slurries
using a diffractometer with Cu Kα radiation to identify themineralogy of the carbonate samples (Tucker & Wright, 1990).

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R. G. JENKINS et al.
produced from each sample by reaction with 100% phosphoricacid in vacuo (25 °C), and analysed with a Finnigan MAT252(Thermo Fisher Scientific Inc., Wattham, MA, USA) mass
spectrometer at EPUT. Carbon and oxygen isotopic values are
expressed relative to the PDB standard. For both carbon andoxygen isotopes, the external precision of the standard was lessthan 0.03‰, with the standards being run at the beginning andthe end of the sample series. Sulphur isotopic analyses were madefrom powdered samples obtained from 1 cm3 carbonate cubes.
The powdered samples were washed with dilute hydrochloric
acid to remove carbonate and sulphate minerals, and thenoxidized from sulphide to sulphate by reaction with concentrated
nitric acid and bromine. Sulphate ions were precipitated as
barite by adding a BaCl2 solution. Sulphur dioxide gas forsulphur isotope analysis was prepared by the V2O5 and SiO2heating methods described by Yanagisawa & Sakai (1983).
Sulphur isotopic composition of the evolved sulphur dioxide gas
was measured with a Finnigan Delta Plus mass spectrometer.
Values of δ34S are reported relative to the CDT scale. The
external precision of the standard for sulphur isotopes was lessthan 0.05‰, with the standards run every twelve samples.

RESULTS
Lithology

Fig. 2 Schematic geological columnar section of the Nakagawa area. Modified
from Takahashi et al. (2003; Fig. 5).

The relative carbonate content of each sample was analysed,
as follows. Powdered samples were heated at 90 °C for 24 h to
dehydrate them, then weighed in quantities of approximately
1 g, and put into centrifuge tubes. One normal hydrochloric
acid was then added to the tubes, which were gently rotatedso as to mix the samples and the acid, in order to dissolve
all the carbonate. This reaction was carried out over 12 h,after which Milli-Q (Millipore, Billerica, MA, USA) water waspoured into the tubes, which were then centrifuged at 400 g
for 50 min. The resulting supernatants were washed, and Milli-Q
was again added to the tubes. The centrifuge process was
repeated at least three times. The tubes with residues werethen dried at 90 °C for more than 12 h. The dried samples
were weighed to calculate their carbonate content.
Powdered samples (about 2 to 10 mg each) obtained by
microdrilling of the small pieces of rock and shell carbonate wereused for carbon and oxygen isotopic analyses. Carbon dioxide was

The geology of the study site is shown in Fig. 1B and consists of mudstone with thin, intercalated sandstone beds. The
sandstone beds are mostly a few centimetre thick (but range
up to 40 cm) and are not cemented, except in the proximityof carbonate bodies. Four such bodies larger than 50 cm indiameter, here named A to D (Fig. 1B), are present at this site.
The largest, and thus the best for tracing lateral changes inlithology and learning its palaeontological content, is CBA(Fig. 3). The lithological and geochemical features of thiscarbonate body and surrounding clastic rocks at YPS are given
in Table 1.
The lithology of CBA can be divided into upper and lower
parts (Fig. 3 A-1). The lower part is composed mainly of
fractured dark grey to greyish black, micritic limestone (Fig. 3),
in association with several layers of fractured sandstone andtuffaceous siltstone. Both brittle and ductile deformation was
exhibited in the fractures. Some peloids, including coatedgrains and networked brown to white calcite rim cement
layers, are evident (Fig. 3F). Micritic limestone in the lower
part has a clotted fabric. Fractured sandstone and tuffaceous
siltstone are cemented by microspar and sparry calcite, or insome cases by siderite. Some of the peloids are coated grains
with nuclei that are enveloped by micritic cement (Fig. 3F).
The nuclei of the coated grains are fractured grey siltstone andfractured tuffaceous siltstone (Fig. 3F). Almost all of the peloids
are covered by radiaxial calcite cement (Fig. 3F). Mostly
medium- to coarse-grained sand-size grains are cemented in
the upper part of CBA, but granule-size grains are sometimes© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Lateral faunal changes in a Late Cretaceous chemosymbiotic assemblage

131

Fig. 3 Outcrop sketch drawing (A) and photographs (B–G) of carbonate body A (CBA) and its lateral extension (YPS). The distance between CBA (A-1) and YPS(A-2) is 5 m, as indicated by the scale at the top. (B) Photograph of a slab sample from sandy mudstone just above CBA. (C) Outcrop photograph of mudstone withnumerous small concretions at YPS. (D) Outcrop photograph of CBA. (E) Outcrop photograph of the 40 cm-thick sandstone bed at YPS. Vertical pipe (conduit pipe)
cuts through the 40 cm-thick sandstone bed. (F) Fractured fabric in the lower part of CBA and a cross-polarized thin-section photograph of coated grains. (G) Slightly
bioturbated mudstone underlying the 40 cm-thick sandstone bed at YPS. Carbon isotope ratios are shown in (C) and (F). The ratios were standardized to PDB.
Abbreviations: c, concretion; bi, bivalve fossil; nc, nuclei; cg, coated grain; rbc, radiaxial bladed calcite cement; sp, sparry calcite; tr, trace fossil. The arrows point
toward the stratigraphically younger strata.

© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

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R. G. JENKINS et al.

Table 1 Meso- and microscopic structures and isotopic characteristics of the carbonate body A (CBA) and its interpreted origin at Yasukawa peripheral site (YPS)
and carbonate body A (CBA) at the Yasukawa site. The isotope ratios are standardized to PDB. AOM: anaerobic oxidation of methane

YPS

CBA

Lower part

Mesoscopic view

Microscopic view

Chemical features

Interpretation

Small concretions

Micrite, clotted fabricPrecipitated by AOM

Fractured greyish
black limestone

Micrite, peloids, coated grains,radiaxial calcite cement,clotted fabricBlocky spar, sparry calcite, sideriteHigh magnesian calcite
δ13C: −40.1 to −39.1‰
δ18O: −2.7 to −2.2‰
Low and high magnesian calcite
δ13C: −43.5 to −39.8‰
δ18O: −2.7 to −0.4‰
Low magnesian calcite
δ13C: −14.5 to −1.8‰
δ18O: −11.3 to −6.2‰
High magnesian calcite
δ13C: −42.0 to −37.7‰
δ18O: −3.1 to −1.9‰
High magnesian calcite
δ13C: −42.0‰
δ18O: −2.5‰
Low magnesian calcite
δ13C: −7.0 to −1.9‰
δ18O: −11.3 to −10.1‰

Fractured sandstone
and taffaceous siltstone
Upper part

Cemented sandstone

Micrite, radiaxial calcite cement

Rim of laterally dispersed
calcite cement layer

Radiaxial calcite cement

Centre of the laterally dispersed
calcite cement layer

Sparry calcite

Precipitated by AOM

Precipitated in latediagenetic stage
Precipitated by AOM

Precipitated by AOM

Precipitated in latediagenetic stage

Fig. 4 (A) Magnesium content of carbonate
body A and surrounding microconcretions at the
Yasukawa site. (B) Carbon and oxygen isotopic
composition of carbonate body A (CBA) and microconcretions just above CBA and at YPS.

present. The upper part of the deposit is characterized bylaterally dispersed layers of calcite cement and networked
brown to white calcite cement. The laterally dispersed calcite
rim-cement is composed of radiaxial-bladed calcite. Sparrycalcite is dominant in the centre of the laterally dispersed
calcite rim-cement layer. No peloids were observed in theupper part. The mudstone just above CBA includes abundantfossils and centimetre-scale micritic concretions (Fig. 3B).
The carbonate content of the lower part of CBA, consisting of
micritic limestone, is 84%, and of the upper part, consisting of
cemented sandstone, is 66%.
The layer of carbonate-cemented sandstone at CBA grades
laterally to non-carbonate cemented sandstone at YPS, where
it bears numerous concretions measuring up to 10 cm indiameter. A vertical conduit-pipe structure cuts through thesandstone bed (Fig. 3E). A considerable number of centimetresize concretions (few mm to 2 cm in diameter) are present in

the overlying mudstone, with some bioturbation but nofracturing evident (Fig. 3C).
Stable isotopic analyses
The data on MgCO3 mole% of CaCO3 solid solution in CBA,
as determined by X-ray diffraction patterns, show a range
from 2 to 12% (Fig. 4A). The carbon and oxygen isotopic
compositions of CBA and small concretions from the YPS are
shown in Fig. 4B. In this report, they are expressed as isotope
ratios versus the PDB standard. The isotopic compositionof micritic limestone, radiaxial calcite rim-cement and small
concretions ranges from −43.5 to −37.7‰ for δ13C and from
−2.7 to −0.4‰ for δ18O. The values for microspar and sparrycalcite cement range from −14.5 to −1.8‰ for δ13C and from
−11.3 to −6.2‰ for δ18O. Aragonitic shells of the bivalve
molluscs, Acharax cretacea and Nanonavis sp., have isotopic© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Lateral faunal changes in a Late Cretaceous chemosymbiotic assemblage
Table 2 Sulphide sulphur isotopic composition at carbonate body A (CBA) andsurrounding clastic rocks at Yasukawa peripheral site (YPS). The sulphur isotopic
composition is expressed relative to the CDT standard in ‰

CBA

YPS

Sample no.

δ34S (‰)

1
2
3
4
5
6
1
2
3
4
5
6

−10.5
9.6
11.0
8.8
−0.5
2.3
−7.0
−6.7
−8.5
−5.1
−7.7
−8.2

values of −3.9 to 0.8‰ for δ13C and −0.5 to 0.8‰ for δ18O.
The sulphur isotopic composition of sulphide from both CBA
and YPS is shown in Table 2. Pyrite extracted from CBA has awide range of δ34S values ranging from −10.5 to 11.0‰ vs.
CDT, whereas pyrite from YPS has a narrow range of −8.5 to−5.1‰ vs. CDT.
Palaeontology
A list of the most common macrofaunal remains extracted
from carbonate body A (including an overlying 15 cm-thickhorizon of sandy siltstone) and YPS is given in Table 3 and133

Fig. 5. CBA and the overlying 15-cm-thick horizon yieldedover 50 specimens of tiny gastropods. Almost all the fossils are
obtained from the non-cemented sediment or micritic limestone.
The most common fossils are unidentified abyssochrysids
whose juveniles (Fig. 5.3) are similar to the Recent provannid
Desbruyeresia melanioides, Ataphridae gen. et sp. indet. (Fig. 5.2)
similar to some species of Recent turbinid Cantrainea, and theacmaeid limpet Serradonta sp. (Fig. 5.1). We also found numerous
small thyasirid and lucinid bivalves (Thyasira sp., Myrtea sp.,and Miltha sp.). Worm tubes (probably vestimentiferans) are
rare. There were no molluscs at YPS, except for ammonoids
in the sandstone layer, which is the lateral equivalent of
the cemented sandstone at CBA. However, gastropods andbivalves are abundant in the overlying mudstone, although lesscommon than at CBA. We also found the solemyoid bivalves
A. cretacea and Nucinella sp., which are rare at CBA. A
detailed taxonomic description of the molluscs found at the
Yasukawa site is in progress.

DISCUSSION
Identification of an ancient methane seep
The negative δ13C values of the micrite, and networked
radiaxial calcite rim-cement indicate that the carbon wasderived from biogenic or thermogenic methane (Whiticar,
1999; Peckmann & Thiel, 2004). It is likely that carbonate
precipitation occurred as a result of increasing alkalinity caused
by AOM (Michaelis et al., 2002; Lein, 2004; Peckmann &Table 3 List of fossils extracted from within and just above carbonate body A (CBA) and surrounding clastic rocks at Yasukawa peripheral site (YPS) at the Yasukawa
site, giving individual numbers and ratios. Note the rarity of Acharax cretacea and Nucinella sp. in the proximity of the methane seep (i.e., CBA). n: number ofindividuals. Each disarticulated bivalve valve is shown in brackets and was counted as half an individual
CBA

YPS

Class

Species

n

%

n

%

Vestimentifera
Gastropoda?vestimentiferan tube
Abyssochrysidae gen. et sp. indet.
Serradonta sp.
Ataphridae gen. et sp. indet.
other gastropods
Acharax cretacea Kanie and NishidaNucinella sp.
Leionucula formosa (Nagao)
Acila (Truncacila) hokkaidoensis (Nagao)
Nuculana (Ezonuculana) mactraeformis Nagao
Propeamussium yubarense (Yabe and Nagao) var.
Myrtea ezoensis (Nagao)
Myrtea sp.
Miltha sp.
Thyasira sp.
Gaudryceras tenuiliratum Yabe
unidentified ammonoids
Fissidentalium cf. otatumei (Nagao)
unidentified decapods
Total

2
19
2
17
5
1
2
0
7 (7)
9 (10)0002
7 (11)
1
1
0
5
94

2.1
20.2
2.1
18.1
5.3
1.1
2.1
0.0
11.2
14.9
0.0
0.0
0.0
2.1
13.3
1.1
1.1
0.0
5.3
###

0
9
0
5
3
9
6 (1)
0 (1)
10 (2)
0
0 (1)
0 (1)
1
1
5 (5)
1
1
3
3
63

0.0
14.4
0.0
8.0
4.8
14.4
10.4
0.8
17.6
0.0
0.8
0.8
1.6
1.6
12.0
1.6
1.6
4.8
4.8
100

Bivalvia

Cephalopoda
Scaphopoda
Crustacea© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

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R. G. JENKINS et al.

Fig. 5 Mollusc fossils from the Yasukawa site. 1a, b. Serradonta sp. lateral (A) and apical (B) views. 2. Ataphridae gen. et sp. indet. 3. Abyssochrysidae gen. et sp.
indet. 4. Thyasira sp. 5. Miltha sp. 6. Myrtea ezoensis. 7. Nucinella sp. 8. Acharax cretacea.

Thiel, 2004). These interpretations are also supported by thepresence of biomarkers typical of the anaerobic methaneoxidizing archaea (e.g., PMI and crocetane with a highly
negative carbon isotope ratio as low as −122‰ vs. PDB) in
the carbonate body (Jenkins, 2006). On the other hand, the13C-enriched isotope ratios in the other carbonate textures(microsparry and sparry calcite cement) at CBA indicate that
all of them were precipitated in the absence of, or with only
inconspicuous amounts of, AOM. Petrographic observations
show that the microsparry and sparry calcite grew during amuch later phase than the micrite and networked radiaxial
calcite rim-cement. In other words, the AOM influence might
have weakened over time during formation of the carbonatebody.
The petrographic and geochemical characteristics of the
Yasukawa carbonate body A are: (1) a high carbonate content
that is comparable in volume to the initial porosity volume ofunconsolidated clastic sediments (Matsumoto, 1978; Ritger

et al., 1987); (2) a high magnesium content (Fig. 4A) similar
to those of carbonates formed under the influence of seawater(Matsumoto, 1978; Ritger et al., 1987); (3) very local in situ
fracturing (Fig. 3), indicating the presence of vigorous fluid
flow and its discharge to the seafloor (Aiello, 2005); (4) anegative sulphur isotopic composition for sulphides, indicating
the influence of bacterial sulphate reduction (Kohn et al.,
1998; Peckmann et al., 2001); and (5) similar oxygen isotope
values for early-diagenetic carbonates and molluscan shellcarbonates, suggesting that both precipitated from isotopicallysimilar water and at almost the same temperatures. These
oxygen isotope values closely resemble the values from Campanian shells of benthic animals examined from outer-shelf
to upper-slope settings in the northwestern Pacific (Moriya
et al., 2003). These characteristics strongly suggest thatthe early-diagenetic carbonates precipitated just below the
sediment/seawater interface in the zone of bacterial sulphate
reduction.
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Lateral faunal changes in a Late Cretaceous chemosymbiotic assemblage

135

Table 4 Summarized lithological and geochemical features of carbonate body A (CBA, the inferred centre of the methane seep) and surrounding clastic rocks at
Yasukawa peripheral site (YPS) (inferred peripheral zone of the methane seep) and their characteristic taxa

Lithology

TextureSize of carbonate

δ34S of sulphide
Typical taxa
Interpretation

CBA

YPS

In situ fractures
2 m in width and 1 m in height−10.5 to 11.0‰
Vestimentiferans and Serradonta
Centre of methane seepNo fractures but weakly bioturbated
Up to 10 cm in diameter concretions−8.5 to −5.1‰
Acharax and Nucinella
Peripheral zone of methane seep

Fossil assemblages from Yasukawa differ from ‘typical’marine fossil assemblages in clastic facies of the Omagari
Formation in both faunal composition and mode of occurrence.
We identified lucinid, thyasirid, and solemyoid bivalves andthe acmaeid gastropod Serradonta, which are typical membersof modern and fossil chemosynthesis-based communities(Reid, 1990; Krueger et al., 1996; Taylor & Glover, 2000;
Warén et al., 2003; Sasaki et al., 2003; Little & Vrijenhoek,
2003; Gill et al., 2005; Kiel & Campbell, 2005; Kiel, 2006).
Molluscs typical of normal-marine (i.e., non-seep) conditionsin the Omagari Formation include the trigoniid Yaadia,
oysters, inoceramids, and ammonoids, all of which occur
allochthonously in sandstone and gravel beds transported bydebris flows or turbidity currents (Takahashi et al., 2003). In
rare cases, nuculoid bivalves such as Acila, Nanonavis, andNuculana (Ezonuculana), and some inoceramids, were foundin situ in the mudstone (Takahashi et al., 2003; A. Takahashi,
pers. com. 2006). Only nuculoid bivalves are common to both
environments.
Centre of the methane seep at Yasukawa
There are several distinctly contrasting lithological and geochemical features between CBA and YPS (see Table 4). First,
the greater amounts of methane-derived calcium carbonate at
CBA strongly suggest that AOM activity was higher at the
precipitation site of the carbonate body than in the surrounding
lithology. Second, in situ fractures occur only at CBA, implyingthat vigorous fluid flow and/or high hydrostatic pressure
typified CBA formation. Third, a variable range of sulphur isotopic compositions at CBA suggests an exhaustion of sulphate
due to bacterial sulphate reduction. This interpretation follows
Peckmann et al. (2001), who attributed varying sulphur isotopic
compositions to a limited incursion of seawater sulphate inpore water, followed by its almost complete consumption due
to bacterial sulphate reduction in a closed system.
Our observations strongly suggest that the concentration of
methane decreased from CBA toward YPS. Furthermore, it isalso probable that the concentration of hydrogen sulphide,probably produced by sulphate-reducing bacteria coupled withanaerobic methane-oxidizing archaea (Orphan et al., 2002),
decreased from CBA toward YPS. Elvert et al. (2005) recently
reported that increasing hydrogen sulphide concentration
indicates an intensive reaction of AOM.
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Pattern of fossil distribution at the Yasukawa methane seep
The Yasukawa site yields moderately rich and relatively
well-preserved fossil assemblages dominated by bivalves andgastropods, compared to other ancient methane-seep localities.
Worm tubes (probably vestimentiferan) are uncommon andfound only in or close to carbonate bodies. In contrast, at thecoeval Omagari site, such tubes are found as mass occurrences(Hikida et al., 2003). This difference apparently reflects thelongevity of the methane seep and/or the strength of its
discharge. The carbonate body containing worm tubes at
the Omagari methane-seep reaches 5 m in height, whereas
the largest carbonate body at the Yasukawa site (CBA) is only
1 m high.
The uncommon occurrence of worm tubes at the Yasukawasite positively correlates with the rarity of Serradonta (Jenkins
et al., in press). This gastropod is a strongly laterally compressed acmaeid limpet known also from Recent methane
seeps around Japan. Its shape is an adaptation for utilizing
vestimentiferan tubes as a substrate (Okutani et al., 1992;
Sasaki et al., 2003). This gastropod is not found in siliciclastic
rocks around the Yasukawa carbonate body A (YPS), but
is very common in the Omagari vestimentiferan rich fossil
methane-seep carbonate. This distribution strongly suggeststhat Serradonta had already evolved to live on vestimentiferantubes by the Cretaceous (Jenkins et al., in press).
The most common gastropods at the Yasukawa site, both at
CBA and at YPS, are unidentified abyssochrysids and ataphrids.
None of the Recent abyssochrysids is known to be a memberof chemosynthetic ecosystems (Bouchet, 1991; Killeen &Oliver, 2000) and, as pointed out by McArthur & Tunnicliffe(1998), they are more likely to be ‘normal’ deep-water
gastropods. On the other hand, most pre-Neogene fossil
abyssochrysids have been found in chemoautotrophy-based
associations. Eocene abyssochrysids are known from Barbados(Kugler et al., 1984; Gill et al., 2005) and the US Pacific
Coast (Squires, 1995; Goedert & Kaler, 1996); in both cases
they were found in ancient methane seeps. Several Mesozoic(Late Jurassic to Early Cretaceous) methane-seep gastropods
from the US Pacific Coast (Stanton, 1895; Campbell & Bottjer,
1993; Campbell et al., 1993) are likely to be abyssochrysids,
although they are described under a variety of names, anda revision is pending. These gastropods are notably
absent from the coeval Omagari site. The reason for such a

136

R. G. JENKINS et al.

distribution remains unclear, but it seems that abyssochrysids
preferred lower concentrations of hydrogen sulphide, since
they are common not only in close proximity to CBA but also
to the more distant YPS. Taking into account the close
relationship of abyssochrysids and provannids, the latter being
typical of chemoautotrophy-based communities, the occurrence of abyssochrysids in ancient methane seeps needs are-evaluation.
Ataphridae, a diverse group of Mesozoic smooth-shelledvetigastropods, have not been reported previously fromancient methane seeps. The exact taxonomic position of thisfamily among Vetigastropoda is still uncertain. Warén (inBouchet et al., 2005) has suggested that ataphrids may represent ancestors of Recent Trochaclididae. Our ataphrids,
however, are more similar to some turbinids and especially tosome species of Cantrainea. Two species of Cantrainea frommodern seeps around Japan were recently described (Okutani& Fujikura, 1990; Okutani, 2001; Sasaki et al., 2005), but theirecology and exact habitat are unknown. The other gastropods
at Yasukawa are rare and their taxonomic description is now inprogress.
The most striking feature of the bivalve assemblage at
the Yasukawa site is the absence of large lucinids, which arereported from the Omagari site (Hikida et al., 2003). Smaller
lucinids are represented by rare Myrtea and Miltha. Living
Myrtea reportedly contains chemoautotrophic bacteria intheir gills (Dando et al., 1985; Taylor & Glover, 2000), but
Recent species are more characteristic of relatively shallow-watersettings rather than methane seeps. Miltha is known fromseveral fossil methane seeps in Japan and New Zealand (seesummary in Campbell, 2006) but is unknown in analogous
modern offshore settings. Thyasirid bivalves are much morecommon. Thyasira is abundant both at CBA and at YPS.
Several species of this genus are reported to contain chemoautotrophic bacteria in their gills (Southward, 1986; Reid,
1990). The distribution of Thyasira sp. at Yasukawa implies
that this species also was chemosymbiotic.
The other bivalves yielding chemoautotrophic bacteria aresolemyoids. At the Yasukawa site, Achatax cretacea (Solemyidae)
and Nucinella sp. (Nucinellidae) were found in both CBA
and the surrounding clastic rocks at YPS (see Table 3; Amanoet al., in press). Acharax is a well-known bivalve that typicallycolonizes peripheral zones of modern methane seeps and hotvents (Sahling et al., 2002; Knittel et al., 2003; Treude et al.,2003), or ancient seeps with diffuse hydrocarbon-rich fluid
flow (Nesbitt & Campbell, 2004). Nucinella is a deep-waterbivalve with a wide but scattered distribution both in Recent
seas and in the fossil record (La Perna, 2005). Judging fromthe absence of a gut in Nucinella (Kuznetsov & Schileyko,
1984), at least some species may rely on chemoautotrophic
bacteria in their life strategy (Reid, 1990). Nucinella isoccasionally found in the vicinity of methane-seep communities(Sasaki et al., 2005). The distribution of solemyoid bivalvesis surprisingly consistent at Yasukawa, where they are rare in

the vicinity of CBA and common in the peripheral clastic
rocks (YPS).
Other bivalves relatively common at the Yasukawa site
include nuculids and nuculanids (Table 3). Recent species ofthese groups are non-chemosymbiotic (Reid, 1990), andpossibly they represent deep-sea generalists in methane-seepsettings. We also regard occurrences of dentalid scaphopods at
YPS as opportunistic, while the presence of ammonoids and asingle shell of a propeamussid bivalve is most probably fortuitous. Finally, remnants of decapods are relatively common in
CBA and YPS, suggesting that these animals could also be
seep related.
The faunal distribution pattern we describe above(abyssochrysids and ataphrids at the methane-seep centre andsolemyoids, Acharax and Nucinella in the peripheral zone)
closely resembles the pattern reported from Hydrate Ridge in
the Cascadia Margin off Oregon by Sahling et al. (2002)
and Knittel et al. (2005). Such a pattern was related by theseworkers to the gradient of hydrogen sulphide concentrations
around a methane seep. A significant difference between
Hydrate Ridge seeps and the Yasukawa seep is the absence ofthe bivalve Calyptogena at the latter. Instead, we encounteredan association of gastropods at the centre of the Yasukawa
methane seep. Possible reasons for this difference are: (1) The
methane discharge at Yasukawa was probably much weaker
than the one at Hydrate Ridge; the size of CBA is just 2 m
in diameter. (2) Calyptogena has been known from dense
accumulations in methane seeps since the Palaeogene, but
only a single specimen of alleged Calyptogena has been reported
from the Omagari methane seep (Hikida et al., 2003). Most
probably, Calyptogena first formed dense populations in the
Eocene (Peckmann et al., 2002). The abyssochrysid- andataphrid-dominated association from the centre of the Yasukawa
methane seep is surprising and requires further studies onother Cretaceous seep associations of Japan.

CONCLUSIONSThe Campanian (Late Cretaceous) carbonate body observedin the Omagari Formation at the Yasukawa site, Nakagawa
area, northern Hokkaido, Japan, is interpreted here as anancient methane-seep deposit on the basis of extremely negative carbon isotope ratios. Methane-bearing pore water rose tonear the seafloor when the methane-derived carbonates wereformed. This interpretation is strengthened by petrographic
observations, showing high carbonate content, the existenceof high-magnesium calcite, in situ fractures, and conduit
structures. The coincidence of sedimentological and petrographic data and the faunal distribution in this chemosynthetic
association also support the hypothesis that the carbonate
bodies were centres of methane discharge, while YPS represents
its peripheral zone. The distribution pattern of the fossils at
Yasukawa roughly corresponds to that observed at modern
methane seeps.
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd

Lateral faunal changes in a Late Cretaceous chemosymbiotic assemblage

ACKNOWLEDGEMENTS
We are deeply grateful to K. Amano (Joetsu University of
Education, Niigata) for his help in identifying some mollusc
fossils. We thank R. Matsumoto, T. Urabe, T. Oji, T. Sasaki,
D. Anton, A. Takahashi, R. Takeuchi, Y. Iba, and K. Kitazawa(all at the University of Tokyo), R. Majima (Yokohama
National University) and T. Nobuhara (Shizuoka University)
for helpful discussions, and three anonymous reviewers fortheir critical and helpful comments. Don Canfield and Kurt
Konhauser are thanked for their editorial efforts. Thanks
are extended to N. H. Landman (American Museum of
Natural History) and J. K. Cochran (Marine Sciences ResearchCentre, State University of New York) for their critical readingof the manuscript. D. C. H. Hikuroa (University of
Auckland), M. E. Jenkins and L. Marincovich (California
Academy of Sciences) are highly appreciated for the linguistic
improvements of the manuscript.
This study was financially supported by scientific research
grants from the Fukada Geological Institute, the Japan Science
Society, the 21st Century COE Program at the University ofTokyo (G3, Leader T. Yamagata), and JSPS grant number
18403013. The research of A. Kaim was supported by theJapan Society for the Promotion of Science (JSPS) Postdoctoral
Fellowship for Foreign Researchers, and JSPS research grant
number 17.05324 (project number 050500000614).

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