Chemosynthesis−based associations on Cretaceous
plesiosaurid carcasses
ANDRZEJ KAIM, YOSHITSUGU KOBAYASHI, HIROKI ECHIZENYA, ROBERT G. JENKINS,
and KAZUSHIGE TANABE
Kaim, A., Kobayashi, Y, Echizenya, H., Jenkins, R.G., and Tanabe, K. 2008. Chemosynthesis−based associations on
Cretaceous plesiosaurid carcasses. Acta Palaeontologica Polonica 53 (1): 97–104.
The objective of this report is to document first Mesozoic occurrences of chemosynthesis−based communities developedon large marine reptile carcasses. Micro−grazing provannid gastropods (typical of chemosynthetic communities) are as−sociated with plesiosaurid skeletons in the Upper Cretaceous deposits of Hokkaido, northern Japan. The cancellous bonesof the examined plesiosaurid bones contain a ubiquity of iron sulfides within the bone trabeculae, which provides evi−
dence of anaerobic sulfate reduction of the bone lipids. We also report numerous microborings in the bone trabeculae,
which might result from the activity of sulfur−oxidizing bacteria. This finding addresses the hotly debated problem of theemergence and radiation of whale bone faunas. We postulate that vertebrate bone environments in the Northwest Pacificregion were settled repeatedly by animals from a regional pool of chemosynthesis−based communities that flourished in
the methane seeps and/or hot vents that were present during the Late Cretaceous–Miocene.
Key wo r d s: Plesiosauridae, Provannidae, vertebrate−bone community, chemosynthetic community, Cretaceous, Japan.
Andrzej Kaim [kaim@twarda.pan.pl], Instytut Paleobiologii PAN, ul. Twarda 51/55, 00−818 Warszawa, Poland and De−
partment of Earth and Planetary Science, University of Tokyo, 7−3−1 Hongo, Bunkyo−ku, Tokyo, 113−0033, Japan;
Yoshitsugu Kobayashi [ykobayashi@museum.hokudai.ac.jp] and Hiroki Echizenya [etizen@museum.hokudai.ac.jp],
Hokkaido University Museum, Kita 10, Nishi 8, Kita−ku, Sapporo, Hokkaido, 060−0810, Japan;
Robert G. Jenkins [robert@eps.s.u−tokyo.ac.jp] and Kazushige Tanabe [tanabe@eps.s.u−tokyo.ac.jp], Department ofEarth and Planetary Science, University of Tokyo, 7−3−1 Hongo, Bunkyo−ku, Tokyo, 113−0033, Japan.

Introduction
The discoveries of hot vent (Lonsdale 1977), cold seep (Paullet al. 1984), and whale bone (Smith et al. 1989) communities
on the bottom of the Recent deep seas has attracted the public
eye by their distinctiveness, high levels of endemicity, andunusual behavioral traits of their animals. The biology, ecol−ogy, and evolution of such communities became a hotly de−bated topic in the scientific world (Smith et al. 1989; Tunni−
cliffe and Juniper 1990; Allison et al. 1991; Martill et al.
1991, 1995; Squires et al. 1991; Hogler 1994; Smith andBaco 2003; Amano and Little 2005; Kiel and Goedert 2006;
Amano et al. 2007). While discussing their emergence andevolution it was hypothesized that large marine reptile car−casses could play a role—as so−called evolutionary steppingstones—in the progressive evolution from normal faunas tohot vent/cold seep communities (Smith et al. 1989; Martill etal. 1991; Distel et al. 2000). Although the existence of such
associations was hypothesized in a number of publications(Martill et al. 1991, 1995; Hogler 1994), supporting fossil ev−
idence remained unknown (Hogler 1994; Kiel and Goedert
2006). Herein we present such a highly anticipated discovery
of a chemosynthesis−based association on marine reptile car−casses.
Acta Palaeontol. Pol. 53 (1): 97–104, 2008

Institutional abbreviations.—EPUT, Department of Earthand Planetary Science, University of Tokyo, Japan; UHR,
Hokkaido University Museum, Sapporo, Japan; ZPAL, Insti−
tute of Paleobiology, Polish Academy of Sciences, Warsaw,
Poland.

Material and methods
We analyzed herein two plesiosaur partial skeletons called
thereafter Turonian skeleton and Coniacian skeleton. The
bones of the Turonian skeleton were mostly extracted fromthe rock matrix by means of mechanical preparation before
beginning this study. However, the portion remaining in therock matrix yielded some gastropod specimens. The skeleton
is identified as a pliosaurid plesiosaur based on a partiallypreserved skull and numerous teeth. The skull length is ap−
proximately 1.5 m, close to the size of a skull of Late Creta−
ceous pliosaur Brachauchenius lucasi estimated to reach up
to 11 m in length (Carpenter 1996).The Coniacian skeleton isstill in preparation, though several mollusk specimens havebeen already recovered. This partial skeleton lacks its skull
and is identified as a plesiosaur due to the presence of nutri−tive foramina for blood vessels on the ventral surface of the
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ACTA PALAEONTOLOGICA POLONICA 53 (1), 2008vertebrae (Storrs 1991). The specimen preserves six dorsal
vertebrae, ribs, gastralia, and the left ilium. The neurocentral
sutures are fused in all preserved vertebrae, indicating that
this individual was an adult. The width of the centrum is ap−
proximately 140 mm, close to the size of vertebrae fromsome Late Cretaceous plesiosaurs ranging 8–12 m in length(Welles 1952). A single tooth of a cow shark was found asso−
ciated with the Coniacian plesiosaur specimen.
Several gastropod specimens have been left attached to
the Coniacian skeleton. Some others have been extracted
from the plesiosaur, coated with platinum, and examined on
Philips XL20 scanning electron microscope at ZPAL. Fourchips of bones detached from Coniacian specimen have been
cut and thin−sectioned at ZPAL laboratory for microscopic
examination. The thin sections were observed and photo−graphed on transmitted light microscopes Olympus BX50 at
ZPAL and Nikon Eclipse E600POL with CCD camera Zeiss
Axio Cam MRc5 at EPUT.

Geological setting
Two plesiosaur partial skeletons have been found in Late
Cretaceous (Turonian and Coniacian) continental slope de−posits of Yezo Group (Okada 1983; Takashima et al. 2004)of the Haboro area, northwest Hokkaido (Fig. 1). Yezo
Group is interpreted as deposits of Cretaceous fore−arc basin
located on the western part of North Pacific margin (Okada
1983; Takashima et al. 2004). The individual of Turonianage (UHR 33108) was found in six boulders dispersed at theleft tributary of the Shirochiunezawa Creek and apparently
derived from the Shirochi Formation (Toshimitsu 1985;
Okamoto et al. 2003). The Shirochi Formation is represented
by intercalations of mudstone and sandstone beds. The sand−stone beds are mostly turbidites and debris flow deposits(Toshimitsu 1985) therefore the formation is interpreted as
deposited on a continental slope.
The Coniacian specimen (UHR 33109) was recoveredfrom a small outcrop at the right bank of the Shirochiune−

Shosanbetsu
Shirachiunezawa

Nakagawa
140°E
44°N

*

Tomamae District
Kanajirisawa
HaboroHa

Hokkaido
Tomamae

Sapporo144°E

Haboro Ward
bo

ro

R.

Na

ut
kah

am

ata

R.

*

Shirachiunezawa

42°N
100 km
10 km

Fig. 1. Sketch maps of Hokkaido, northern Japan (A) and Tomamae District(B) with discussed localities indicated.

zawa Creek about 250 m down of the Turonian specimen.
The locality crops out siltstones of Lower Haborogawa For−mation. The formation is represented mainly by gray to darkgray massive siltstone (Okamoto et al. 2003) and displays
upward−coarsening of the sediment (Okamoto et al. 2003).
This feature is interpreted as a regressive trend leading to achange from continental slope to outer shelf setting. Accord−
ing to Okamoto et al. (2003), Haborogawa Formation (lower
and upper parts) corresponds to Nishichirashinai, Omagari,and Osoushinai Formations in Nakagawa area of the north−ern Hokkaido. The Santonian–Campanian Omagari Forma−tion is known to yield several methane−seep associations(Hikida et al. 2003; Jenkins et al. 2007a, b).

Mollusks associated to plesiosaur
skeletons
The rock matrix remaining in the Turonian skeleton yielded
eight specimens of melanoid−shaped gastropods with strong
axial and spiral sculpture. The Coniacian skeleton provided
36 specimens of similar gastropods, two specimens of veti−
gastropods, and eight bivalve fragments. The fossil inverte−
brates were found adjacent to the bone (Fig. 2J) or in its im−
mediate proximity (usually less than 50 mm). Most of thegastropod specimens in the Coniacian plesiosaur are concen−
trated in the cavity of the posterior part of the dorsal verte−brae (Fig. 2A). Some other specimens were found in thecrevices between the centra (Fig. 2H–K). These specimens
are preserved with original shell microstructure and appar−
ently were not significantly affected by diagenesis, though
their juvenile whorls are missing.
The melanoid−shaped gastropods are represented by atleast two species (Fig. 3A, E, F, J, K). One of the species (Fig.
3A) is very similar to a new species of Desbruyeresia (Fig. 3B,C) described by Kaim et al. (in press), from the Cenomanianmethane seep deposits in the Kanajirisawa Creek, Tappu area,
about 30 km south of the Haboro plesiosaur localities (Fig.
1A). The provannids at the Kanajirisawa appear in mass
occurrences and some of the specimens preserve decollate
protoconchs (Fig. 3C), which are typical of these gastropods(Warén and Bouchet 1993). Another gastropod species (Fig.
3D) from the Turonian skeleton is very similar to a Campanianprovannid (Fig. 3I) reported by Kaim et al. (in press) from the
Nakagawa area (Fig. 1), northern Hokkaido (50 km NE fromthe plesiosaur localities). The species from locality Gakkono−sawa exhibits the same type of macro− and microornamen−tation. The differences between specimens from plesiosaurbones and from methane seeps of adjacent areas seem to be of
only specific importance. The only similar gastropods which
could by misidentified as provannids are cerithiids. However,cerithiids have a very different protoconch. Such gastropods
have never been found in the methane seeps of Japan. More−over, in modern seep/vent faunas worldwide there is only asingle published record of cerithiid gastropods: Lirobittium is

KAIM ET AL.—PLESIOSAUR−BONE ASSOCIATIONS FROM JAPAN99

Fig. 2. Plesiosaur bones from the Coniacian slope deposits of Shirochiunezawa Creek, Haboro area of Hokkaido, Japan. A. Whole specimen UHR 33109 indorsolateral view preserving four dorsal vertebrae and left ilium with gastropods (yellow circles) and bivalves (blue circles) embedded in the rock matrix in thebone cavities. Asterisked specimen is from Fig. 3A. B. Thin section of the bone (b; black in crossed polars); the bone is embedded in a carbonate matrix (mot−tled) containing some siliciclastic grains. Note a part of the bone in between the arrows that was totally disintegrated by possible bacterial activity. C. Clottedfabric (cl for cloths) in micritic matrix surrounded by sparry calcite (sp), b for bone. D. A section through cancellous bone showing thin layer of cement contain−
ing framboidal pyrite (py and arrow) and overgrown by radiaxial calcite cement (rcc); sp is for sparite. E. A section through cancellous bone showing trabecular
structure; pcl (pyrite concentration layer) indicates the 7 mm−thick layer within the bone periphery that is enhanced by iron sulfide. F. Thin section through abone trabecula (b; yellow) with framboidal crystals of iron sulfide (opaque); the bone is embedded in sparry calcitic cement (grey). G. Trabecula (b) withheavily bored tip by possible bacterial activity. H. Ventral view of centra (anterior to the right) with provannid gastropods indicated by p. I. Anterior view of 6th
and a part of 5th centra detached from the specimen on A and H. J Magnified fragment from I showing position of the provannid gastropod. K. Magnification ofa cavity from A showing position of provannids (p), unidentified bivalve (bv), and inoceramid Inoceramus uwajimensis (inc).
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ACTA PALAEONTOLOGICA POLONICA 53 (1), 2008

Fig. 3. Gastropods from the Late Cretaceous plesiosaur bones and seeps of Hokkaido, Japan. A, E, J. Provannidae gen. et sp. indet. 1 (UHR 33109m1, UHR
33109m2, and UHR 33109m3 respectively) from the Coniacian plesiosaurid bone association at Shirochiunezawa Creek (Haboro area), very similar toa new species of Desbruyeresia (B, C) from the Cenomanian methane seep deposits of Kanajirisawa Creek (Tappu area), UMUT MM29355 and UMUT
MM29357 respectively (described in detail by Kaim et al. in press). C. Specimen UMUT MM29357 possesses a decollate protoconch typical ofProvannidae. D. Provannidae gen. et sp. indet. 3 (UHR 33110m1) from the Turonian plesiosaurid bone association at Shirochiunezawa Creek, very similar
to an undescribed provannid (I) from the Campanian methane seep deposits at Gakkonosawa Creek (Nakagawa area), UMUT MM29364; similar or thesame species (K) is also found in the Coniacian plesiosaurid bone association at Shirochiunezawa Creek (Haboro area), UHR 33109m4. F. Provannidae
gen. et sp. indet. 2 from Coniacian plesiosaurid bone association at Shirochiunezawa Creek (Haboro area), UHR 33109m5. G. Outer mould ofvetigastropod gen. et sp. indet (UHR 33109m6) from Coniacian plesiosaurid bone association at Shirochiunezawa Creek (Haboro area), very similar to an
ataphrid gastropod (H) from the Campanian methane seep deposits at Omagari (Nakagawa area), UMUT unregistered specimen.

recorded from seeps off California by Levin et al. (2000).
There are no undoubted cerithiids from fossil hot vents andcold seeps. It seems that cerithiids are just now on their way tochemosynthesis−based communities. Cerithiids are also un−
known from the continental slope deposits in the Cretaceousof Japan. They are known only from shallow−water sediments(Nagao 1932, 1939; Nagao and Ôtatume 1938; Hayami andKase 1977; Kase 1984). Therefore, taking into account allabove we interpret the melanoid−shaped gastropods as speciesof Provanna and Desbruyeresia (both Provannidae) thoughdiagnostic protoconchs have not been preserved in specimensfrom plesiosaurs.
The vetigastropod (Fig. 3G; nacreous layer is present)
associated with the plesiosaur bones morphologically resem−
bles ataphrid−like gastropods (Fig. 3H), which are common
in the methane seep deposits of the Nakagawa area (Jenkins
et al. 2007a, b). The remnants of the bivalves found at thebones are poorly preserved and we could identify only asingle specimen of an inoceramid Inoceramus uwajimensis
Yehara, 1924 (Fig. 2K).

Petrographic and microstructuralfeatures of the plesiosaur specimens
The plesiosaur bones under consideration display trabecular
structure (Fig. 2E) similar to those known from the whalebones. This structure is considered an adaptation to a fully
aquatic mode of life (Ricqlès and Buffrénil 2001). The mar−row spaces between the trabeculae are filled with sparrycalcitic cement (Fig. 2F) or carbonate matrix (Fig. 2B, G)
containing some unidentified clay minerals. Some parts ofthe matrix display clotted fabric (Fig. 2C), which is primarilya microbial feature (e.g., Riding 2000; Peckmann and Thiel
2004). Moreover, some bone trabeculae are covered by alayer of banded botryoidal−like radiaxial calcitic cements(Fig. 2D). This might be a Cretaceous counterpart of ara−
gonitic botryoidal cements which are believed to be linked tomicrobial activity (Teichert et al. 2005; Peckmann et al.
2007). These petrographic features are commonly found inancient and Recent methane seep deposits (e.g., Greinert etal. 2002; Campbell et al. 2002; Peckmann and Thiel 2004).
The 7 mm thick layer (pcl in Fig. 2E) within the bone periph−
ery is enhanced in iron sulfide coating trabeculae surfaces ina similar manner to the Recent whale bones (Allison et al.
1991). Thin sections made from a bone chip from the Conia−
cian specimen at Shirochiunezawa revealed numerous oc−
currences of framboidal pyrite crystals (up to 25 μm in diam−eter) on the surface of the bone with some of the trabeculae
covered by pyrite layers of variable thickness (Fig. 2F). The
outer bone surfaces are extensively bored, exhibited by cy−lindrical holes (Fig. 2B, G) with an average diameter of 5 μm
and a length of up to 100 μm. At some places the bone is to−tally disintegrated by the borings (Fig. 2B). Similar struc−

KAIM ET AL.—PLESIOSAUR−BONE ASSOCIATIONS FROM JAPANtures and degree of disintegration have been reported from
Miocene whale falls (Amano and Little 2005; Amano et al.
2007). Amano and Little (2005: 352) stated that micro−
borings “fall into the size range of microborings made by al−gae, bacteria and fungi” but simultaneously they interpretthese borings as “possibly microbial” (Amano and Little
2005: 345) and furthermore they compare them to the bor−
ings reported from the modern whale bones by Deming et al.
(1997). Amano et al. (2007: 240) subsequently infer “puta−tive bacterial mats (for which we have no direct evidence) on
the bones and surrounding sediment surface. These mats
may have been grazed by Provanna? sp.”. Regrettably, themicroborings are poorly documented from Recent whale car−casses being restricted to the figure 5c in Allison et al.
(1991). It seems, however, sufficient to compare the micro−
borings reported from Oligocene (conference abstract ofSpangler and Shapiro 2007 that needs confirmation in a peer
reviewed journal) and Miocene (Amano and Little 2005;
Amano et al. 2007) whale falls, and Cretaceous plesiosaur
falls (this paper) with the “small tubes” described by Allison
et al. (1991: 80) from Recent whale falls. Allison et al. (1991)
did not provide any evidence as for the origin of these micro−
borings, however, Deming et al. (1997) reported a high con−centration of bone penetrating bacteria—with predominanceof submicron−sized cocci and less frequent rod−shaped forms—in the peripheral region of the Recent whale bone. More−over, the density of the bacteria is negatively correlated withlipid content of the bone (Deming et al. 1997) which suggeststhat the bacterial community is fuelled by the lipids. Simulta−
neously, Deming et al. (1997) reported also a dense commu−
nity of microbial mats composed mainly of filamentous bac−teria with minor component of rods and cocci. Deming et al.
(1997) did not suggest any connection between microtubes
reported by Allison et al. (1991) and examined bacteria but
no other organisms viable to perform such borings were re−ported neither by Allison et al. (1991) nor Deming et al.
(1997). It seems therefore to be sound to argue that the
microborings and bacteria in Recent whale bones are related
each other.
Although we have no direct evidence of the bacterial originof the borings in plesiosaur bones as they fall into size range ofboring made not only by bacteria but also algae and fungi(compare e.g., Underwood et al. 1999; Vogel and Marinco−
vich 2004; Wisshak et al. 2005), nevertheless they are analo−
gous to the structures reported from both Recent whale falls(Allison et al. 1991) and we conclude that it is most parsimoni−
ous to interpret them as traces of bacterial activity until anotherorigin of Recent borings in whale falls is reported. Further
work on the morphology and identity of the borings from fos−sil both whale and plesiosaur bones is pending as similar struc−tures are known also from fish teeth (Underwood et al. 1999)
and sirenian bones (Astibia et al. 2005).
The presence of pyrite layers within the bone peripheryand the trabeculae suggests anaerobic microbial decomposi−tion of the bone organic compounds (lipids), resulting in sul−fate reduction and the release of the sulfides into the local en−

101

vironment (Allison et al 1991; Deming et al. 1997; Amanoand Little 2005; Amano et al. 2007). It remains unclear if tiny
provannids from the plesiosaur bones had bacterial symbi−
onts, as the latter are reported so far only from the large
provannids (Warén and Bouchet 1993; Desbruyères et al.
2006) and small species have yet to be examined in this re−spect (Anders Warén, personal communication 2007). Nev−
ertheless our provannids were probably grazing upon puta−tive bacterial mats as do their Recent counterparts (Warén
and Bouchet 1993; Desbruyères et al. 2006). The presence ofa bacterial mat and its grazers on plesiosaur carcasses may
correspond to the sulfophilic stage in the ecological succes−
sion of whale fall communities (Bennett et al. 1994; Smithand Baco 2003; Kiel and Goedert 2006; Smith 2007). Thissuggests that plesiosaur carcasses, similar to their whalecounterparts, may have passed through similar ecologicalsuccessional stages (i.e., a mobile scavenger stage, an enrich−ment opportunistic stage, and a sulfophilic stage). Such a
scenario has been predicted theoretically (Martill et al. 1991,
1995; Hogler 1994) for large marine reptiles but never ad−
dressed by reliable fossil evidence (Hogler 1994; Kiel and
Goedert 2006).

Discussion
The fossil record of whale fall communities is extremely
scarce and limited to Japan and US Pacific Coast (Goedert etal. 1995; Amano and Little 2005; Kiel and Goedert 2006;
Amano et al. 2007). Kiel and Godert (2006) argue that theoldest−known whale falls (Eocene–Oligocene) from the US
Pacific Coast lacked the sulfophilic stage, preserving rather a“chemosymbiotic opportunistic stage”. The latter stage “…ischaracterized by species from wood−falls and from the back−ground fauna which are adapted to reducing environments
and most likely took advantage of elevated sulfide levels inthe sediments underneath and around the whale carcass,rather than from anaerobic breakdown of bone lipids” (Kieland Goedert 2007: 2629). After examination of faunal com−position in these associations Kiel and Goedert (2006) con−cluded that the bones of primitive, small−bodied Oligocene–
Eocene whales provided too small amount of oil to sustainorganisms typical of the sulfophilic stage. This supposition,
however, has been weakened recently by Pyeson and Haasl(2007), who have discovered a small whale fossil from Mio−
cene rocks from California that is closely associated withvesicomyid bivalves. Moreover, Spangler and Shapiro (2007)
argue in a conference abstract that whale bones from the
Oligocene locality at the Sekiu River (Kiel and Goedert
2006) provided several features indicating bacterial degrada−tion of the bones. If confirmed in a peer reviewed journal it
might indicate that also Oligocene–Eocene whale falls could
sustain communities at sulfophilic stage although impover−ished in the taxonomic composition. Undoubted whale bonecommunities that preserve the faunal association typical of
sulfophilic stage are those known from the Miocene of Japan
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102(Amano and Little 2005; Amano et al. 2007). These associa−
tions consists of fauna typical of whale bone communities in−cluding Adipicola, Calyptogena, and Provanna (Amano andLittle 2005; Amano et al. 2007).
Our plesiosaur skeleton did not provide any of the large
mytilid and/or vesicomyid bivalves which rely fully or partly
on sulphide−oxidizing endosymbionts and characterize the‘sulfophilic stage‘ in the whale bone community. However,recent investigations (Amano and Kiel 2007) have not con−firmed any of the large vesicomyids from the Cretaceous
methane seeps in Japan. The bivalves reported by Kanie andvarious co−workers (Kanie et al. 1993, 1996, 2000; Kanie
and Kuramochi 1996; Kanie and Nishida 2000) and Hikida
et al. (2003) appear to be rather lucinids (Amano and Kiel
2007). Moreover, even these bivalves are rather uncommon
in the Cretaceous methane seeps. For example, there is onlya single large bivalve specimen from large methane seep car−bonate at Omagari (Hikida et al. 2003; own investigations).
Therefore, it is no wonder that they were not discovered at
plesiosaur carcasses. We found a few shells of small bivalves
and all but one inoceramid are non−identifiable because of
the preservation state. We believe that further investigations
will reveal also plesiosaur fall associations with bivalves typ−ical at chemosynthesis−based communities.
The relatively large number of provannids associatedwith ataphrid−like vetigastropods from plesiosaur bone asso−
ciations corresponds well to the similar but better diversified
Late Cretaceous methane seep associations known from ad−
jacent areas (Jenkins et al. 2007a, b; see also Hikida et al.
2003). Miocene whale fall associations from Japan display
similar patterns of taxonomic composition to the contempo−
rary methane seeps (Amano et al. 2007). The impoverishedtaxonomic composition of plesiosaur fall communities andtheir similarity to much more diversified coeval methane
seep communities may suggest that the vertebrate fall com−munities have been established several times by immigrants
from other chemosynthesis−based communities when appro−
priately sized vertebrate carcasses appeared at deep sea floor.
Such a conclusion is supported by our findings of plesiosaurbone associations exclusively in the vicinity of other chemo−
synthesis−based communities.
The finding of chemosynthesis−based communities on
plesiosaur falls addresses also the idea of vertebrate bones
acting as evolutionary and dispersal stepping stones (Smithet al. 1989; Martill et al. 1991; Distel et al. 2000). Taking into
account similarity of plesiosaur communities to synchronous
seep communities we may suppose that the former could act
as stepping stones between some methane seeps. The impov−
erished taxonomic composition of plesiosaur bone associa−
tions may suggest that their evolutionary importance in de−velopment of chemosynthesis−based communities (at least
methane seeps) might be limited. However, with the material
at hand it is difficult to argue if our findings document ‘incip−
ient’ or opportunistic colonization of a sulphide−rich sub−strate from adjacent cold seeps that was not repeated geo−
graphically or temporally until the evolution of whales in the

ACTA PALAEONTOLOGICA POLONICA 53 (1), 2008

Eocene or it is just the negligence of vertebrate paleontolo−
gists who do not pay attention for tiny mollusks associatedwith large skeletons. Another factor which has to be taken
into consideration is a diagenetic alteration of the calcareous(especially aragonitic) shell material in localities wherebones are well preserved. Nevertheless we feel confident that
careful studies on skeletons from rock formations yielding
also cold seep associations will provide additional reptile
bone associations.

Conclusions
Two dozen−meter large plesiosaurid skeletons (one pliosaur
and one plesiosaur) from Upper Cretaceous deep water de−posits of Japan are associated with chemosynthesis−based as−sociations of invertebrates. The composition of the associa−
tions strongly recollects coeval methane seep associations
from the same area, though the former being impoverished in
the taxonomic composition. Several petrographic features
obtained from bone thin sections, e.g., clotted fabric, banded
botryoidal−like radiaxial calcitic cements, framboidal pyrite
crystals arranged in layers covering bone trabeculae, and pe−ripheral bone layer enhanced in sulfide coatings, strongly
suggest bacterial activity analogous to the one reported frommodern examples of whale bone communities. The cylindri−cal holes extensively penetrating the outer bone surfaces may
be interpreted as bacterial in origin although fungal affilia−tion is also possible. Further investigations on this matter are
still pending.
Our findings indicate that vertebrate fall communities
could develop several times in the geological past not only on
whale falls but also on marine Mesozoic reptiles. The similar−
ity of the plesiosaur bone and coeval methane seep associa−
tions strongly supports the idea that vertebrate bones could act
as dispersal stepping stones for chemosynthesis−based com−munities, at least in the Late Cretaceous. There is still noenough data to argue about the role of reptile fall communities
in the evolution of chemosynthesis−based communities. We
expect a number of further discoveries of reptile bone associa−
tions from the regions yielding fossils of other types (espe−
cially methane seeps) of chemosythesis−based associations.

Acknowledgements
We thank Brian M. Davis (Oklahoma Museum of Natural History,
Norman, USA) for linguistic adjustment. Andrzej Pisera and Zbi−
gniew Strąk (both ZPAL) are acknowledged for help in preparing andphotographing thin sections. The research of A.K. was supported by
the Japan Society for the Promotion of Science (JSPS) Postdoctoral
Fellowship for Foreign Researchers and associated research grant
number 17.05324 (project number 050500000614). A.K., R.G.J., andK.T. were supported by JSPS grant no. 18403013. The paper greatly
benefited from critical comments from James L. Goedert (Universityof Washington, Seattle, USA), Craig R. Smith (University of Hawaii
at Manoa, Honolulu, USA) and four anonymous reviewers.

KAIM ET AL.—PLESIOSAUR−BONE ASSOCIATIONS FROM JAPAN

References
Allison, P.A., Smith, C.R., Kukert, H., Deming, J.W., and Bennett, B.A.
1991. Deep−water taphonomy of vertebrate carcasses: a whale skeleton
in the bathyal Santa Catalina Basin. Paleobiology 17: 78–89.
Amano, K. and Kiel, S. 2007. Fossil vesicomyid bivalves from the North Pa−
cific region. Veliger 49: 270–293.
Amano, K. and Little, C.T.S. 2005. Miocene whale−fall community from
Hokkaido, northern Japan. Palaeogeography, Palaeoclimatology, Palaeo−
ecology 215: 345–356.
Amano, K., Little, C.T.S., and Inoue, K. 2007. A new Miocene whale−fallcommunity from Japan. Palaeogeography, Palaeoclimatology, Palaeo−
ecology 247: 236–242.
Astibia, H., Payros, A., Pereda Superbiola, X., Elorza, J., Berreteaga, A.,
Etxebarria, N., Badiola, A., and Tosquella, J. 2005. Sedimentology andtaphonomy of sirenian remains from the Middle Eocene of the Pam−
plona Basin (Navarre, western Pyrenees). Facies 50: 463–475.
Bennett, B.A., Smith, C.R., Glaser, B., and Maybaum, H.L. 1994. Faunal
community structure of a chemoautotrophic assemblage on whalebones in the deep northeast Pacific Ocean. Marine Ecology Progress
Series 108: 205–223.
Campbell, K.A., Farmer, J.D., and Des Marais, D. 2002. Ancient hydrocar−
bon seeps from the Mesozoic convergent margin of California: carbon−
ate geochemistry, fluids and palaeoenvironments. Geofluids 2: 63–94.
Carpenter, K. 1996. A review of short−necked plesiosaur from the Creta−
ceous of the Western Interior, North America. Neues Jahrbuch für
Geologie und Paläontologie Abhandlungen 201: 259–287.
Deming, J.W., Reysenbach, A.L., Macko, S.A., and Smith, C.R. 1997. Evi−dence for the microbial basis of a chemoautotrophic invertebrate com−munity at a whale fall on the deep seafloor: bone−colonizing bacteria
and invertebrate endosymbionts. Microscopy Research and Technique
37: 162–170.
Desbruyères, D., Segonzac, M., and Bright, M. (eds.) 2006. Handbook of
Deep−sea Hydrothermal Vent Fauna (second edition). 544 pp. Biologie−
centrum der Oberösterreichische Landesmuseum, Linz.
Distel, D.L., Baco, A.R., Chuang, E., Morrill, W., Cavanaugh, C., andSmith, C.R. 2000. Do mussels take wooden steps to deep−sea vents? Na−ture 403: 725–726.
Goedert, J.L., Squires, R.L., and Barnes, L.G. 1995. Paleoecology ofwhale−fall habitats from deep−water Oligocene rocks, Olympic Penin−
sula, Washington state. Palaeogeography, Palaeoclimatology, Palaeo−
ecology 118: 151–158.
Greinert, J., Bohrmann, G., and Elvert, M. 2002. Stromatolitic fabric ofauthigenic carbonate crusts: result of anaerobic methane oxidation atcold seeps in 4,850 m water depth. International Journal of Earth Sci−
ences 91: 698–711.
Hayami, I. and Kase, T. 1977. A systematic survey of the Paleozoic and Me−
sozoic Gastropoda and Paleozoic Bivalvia from Japan. The University
Museum, The University of Tokyo, Bulletin 13: 1–156.
Hikida, Y., Suzuki, S., Togo, Y., and Ijiri, A. 2003. An exceptionallywell−preserved fossil seep community from the Cretaceous Yezo Groupin the Nakagawa area, Hokkaido, northern Japan. Paleontological Re−
search 7: 329–342.
Hogler, J.A. 1994. Speculations on the role of marine reptile deadfalls in
Mesozoic deep−sea paleoecology. Palaios 9: 42–47.
Jenkins, R.G., Kaim, A., and Hikida, Y. 2007a. Antiquity of the substratechoice among acmaeid limpets from Late Cretaceous chemosynthesis−
based communities. Acta Palaeontologica Polonica 52: 369–373.
Jenkins, R.G., Kaim, A., Hikida, Y., and Tanabe, K. 2007b. Methane flux
dependent lateral faunal changes in a Late Cretaceous chemosymbiotic
assemblage from the Nakagawa area of Hokkaido, Japan. Geobiology 5:
127–139.
Kaim, A., Jenkins, R.G., and Warén, A. (in press). Provannid and provannid−
like gastropods from the Late Cretaceous cold seeps of Hokkaido (Japan)
and the fossil record of the Provannidae (Gastropoda: Abyssochrysoidea).
Zoological Journal of the Linnean Society.

103

Kanie, Y. and Kuramochi, T. 1996. Description of possibly chemosynthetic
bivalves from the Cretaceous deposits of the Obira−cho, northwestern
Hokkaido. Science Report of the Yokosuka City Museum 44: 63–68.
Kanie, Y. and Nishida, T. 2000. New species of chemosynthetic bivalves,
Veiscomya and Acharax, from the Cretaceous deposits of northwestern
Hokkaido. Science Report of the Yokosuka City Museum 47: 79–84.
Kanie, Y., Nishida, T., Kuramochi, T., and Kawashita, Y. 2000. Chemo−
synthetic bivalve community discovered from the Cretaceous depositsin Horokanai−cho, northwestern Hokkaido. Science Report of the Yoko−suka City Museum 47: 73–78.
Kanie, Y., Yoshikawa, Y., Sakai, T., and Kuramochi, T. 1996. Cretaceous
chemosynthetic fauna from Hokkaido. Science Report of the Yokosuka
City Museum 44: 69–74.
Kanie, Y., Yoshikawa, Y., Sakai, T., and Takahashi, T. 1993. The Creta−
ceous chemosynthetic cold water−dependent molluscan community
dicovered from Mikasa City, central Hokkaido. Science Report of the
Yokosuka City Museum 41: 31–36.
Kase, T. 1984. Early Cretaceous marine and brackish−water Gastropoda
from Japan. 263 pp. National Science Museum, Tokyo.
Kiel, S. and Goedert, J.L. 2006. Deep−sea food bonanzas: early Cenozoic
whale−fall communities resemble wood−fall rather than seep communi−ties. Proceedings of the Royal Society of London Series B−Biological
Sciences 273: 2625–2631.
Levin, L.A., James, D.W., Martin C.M., Rathburn, A.E., Harris, L.H., andMichener, R.H. 2000. Do methane seeps support distinct macrofaunalassemblages? Observations on community structure and nutrition fromthe northern California slope and shelf. Marine Ecology Progress Series
208: 21–39.
Lonsdale, P. 1977. Clustering of suspension−feeding macrobenthos nearabyssal hydrothermal vents at oceanic spreading centers. Deep−Sea Re−
search 24: 857–863.
Martill, D.M., Cruickshank, A.R.I., and Taylor, M.A. 1991. Dispersal via
whale bones. Nature 351: 193.
Martill, D.M., Cruickshank, A.R.I., and Taylor, M.A. 1995. Speculations on
the role of marine reptile deadfalls in Mesozoic deep−sea paleoecology:
comment: Palaios 10: 96–97.
Nagao, T. 1932. Some Cretaceous Mollusca from Japanese Saghalin andHokkaido (Lamellibranchiata and Gastropoda). Journal of the Facultyof Science, Hokkaidô Imperial University, Series IV, Geology and Min−
eralogy 2: 23–50.
Nagao, T. 1939. Some molluscan fossils from the Cretaceous deposits of
Hokkaido and Japanese Saghalien. Journal of the Faculty of Science,
Hokkaidô Imperial University, Series IV, Geology and Mineralogy 4:
214–239.
Nagao, T. and Ôtatume, K. 1938. Molluscan fossils of the Hakobuti sand−stone of Hokkaidô. Journal of the Faculty of Science, Hokkaidô Impe−
rial University, Series IV, Geology and Mineralogy 4: 31–56.
Okada, H. 1983. Collision orogenesis and sedimentation in Hokkaido, Ja−pan. In: M. Hashimoto and S. Uyeda (eds.), Accretion Tectonics in the
Circum−Pacific Regions, 91–105. Terra Scientific Publishing Com−pany, Tokyo.
Okamoto, T., Matsunaga, G., and Okada, M. 2003. Restudy of the Upper
Cretaceous stratigraphy in the Haboro area, northwestern Hokkaido.
Journal of Geological Society of Japan 109: 363–382.
Paull, C.K., Hecker, B., Commeau, R., Freeman−Lynde, R.P., Neumann, C.,
Corso, W. P., Golubic, S., Hook, J. E., Sikes, E., and Curray, J. 1984. Bi−
ological communities at the Florida Escarpment resemble hydrothermalvent taxa. Science 226: 965–967.
Peckmann, J., Campbell, K.A., Walliser, O.H., and Reitner, J. 2007. A Late
Devonian hydrocarbon−seep deposit dominated by dimerelloid brachio−
pods, Morocco. Palaios 22: 114–122.
Peckmann, J. and Thiel, V. 2004. Carbon cycling at ancient methane−seeps.
Chemical Geology 205: 443–467.
Pyenson, N.D and Haasl, D.M. 2007. Miocene whale−fall from California
demonstrates that cetacean size did not determine the evolution of mod−ern whale−fall communities. Biology Letters 3: 709–711.
Ricqlès, A. de and Buffrénil, V. de 2001. Bone histology, heterochronies
http://app.pan.pl/acta53/app53−097.pdf

104
and return of tetrapods to life in water: were are we? In: J.−M. Mazin and
V. de Buffrénil (eds.), Secondary Adaptations of Tetrapods to Life in
Water, 289–310. Verlag Dr. Friedrich Pfeil, München.
Riding, R. 2000. Microbial carbonates: the geological record of calcified
bacterial−algal mats and biofilms. Sedimentology 47 (Supplement 1):
179–214.
Squires, R.L., Goedert, J.L., and Barnes, L.G. 1991. Whale carcasses. Nature
349: 574.
Smith, C.R. 2007. Bigger is better: The role of whales as detritus in marine
ecosystems. In: J.A. Estes, D.P. DeMaster, D.F. Doak, T.M. Williams,
and R.L. Brownel (eds.), Whales, Whaling and Ocean Ecosystems,
286–300. University of California Press, Berkeley.
Smith, C.R. and Baco, A.R. 2003. Ecology of whale falls at the deep−sea
floor. Oceanography and Marine Biology: an Annual Review 41:
311–354.
Smith, C.R., Kukert, H., Wheatcroft, R.A., Jumars, P.A., and Deming, J.W.
1989. Vent fauna on whale remains. Nature 341: 27–28.
Spangler, E. and Shapiro, R. 2007. New evidence of bacterial degradation infossil whale falls: not just a boring tale! GSA Cordilleran Section—103rd
Annual Meeting, Bellingham, Washington. http://gsa.confex.com/gsa/
2007CD/finalprogram/abstract_121147.htm.
Storrs, G.W. 1991. Anatomy and relationships Corosaurus alcovensis(Diapsida: Sauropterygia) and the Triassic Alcova Limestone of Wyo−ming. Bulletin of the Peabody Museum of Natural History 44: 1–151.
Takashima, R., Kawabe, F., Nishi, H., Moriya, K., Wani, R., and Ando, H.
2004. Geology and stratigraphy of forearc basin sediments in Hokkaido,

ACTA PALAEONTOLOGICA POLONICA 53 (1), 2008
Japan: Cretaceous environmental events on the north−west Pacific mar−gin. Cretaceous Research 25: 365–390.
Teichert, B.M.A., Bohrmann, G., and Suess, E. 2005. Chemoherms on Hy−
drate Ridge—Unique microbially−mediated carbonate build−ups growing
into the water column. Palaeogeography, Palaeoclimatology, Palaeo−
ecology 227: 67–85.
Toshimitsu, S. 1985. Biostratigraphy and depositional facies of the Creta−
ceous in the upper reaches of the Haboro River, Hokkaido. Journal of
Geological Society of Japan 91: 599–618.
Tunnicliffe, V. and Juniper, S.K. 1990. Cosmopolitan underwater fauna.
Nature 344: 300.
Underwood. C.J., Mitchell, S.F., and Veltkamp, C.J. 1999. Microborings in
mid−Cretaceous fish teeth. Proceeding of the Yorkshire Geological So−
ciety 52: 269–274.
Vogel, K. and Marincovich, L. 2004. Paleobathymetric implications of
microborings in Tertiary strata of Alaska, USA. Palaeogeography,
Palaeoclimatology, Palaeoecology 206: 1–20.
Warén, A. and Bouchet, P. 1993. New records, species, genera, and a new
family of gastropods from hydrothermal vents and hydrocarbon seeps.
Zoologica Scripta 22: 1–90.
Welles, S.P. 1952. A review of the North American Cretaceous elasmosaurs.
Univeristy of California Publications in Geological Sciences 29: 47–144.
Wisshak, M., Gektidis, M., Freiwald, A., and Lundälv, T. 2005. Bioerosion
along a bathymetric gradient in a cold−temperate setting (Kosterfjord,
SW Sweden): an experimental study. Facies 51: 93–117.