Age and Growth of Glossocardia obesa, a "Large" Bivalve in a Submarine Cave Within a Coral Reef, as Revealed by Oxygen Isotope Analysis

2011·3.4 MB·English

by  Akihisa Kitamura

THE VELIGER
©CMS,
The Veliger 51(2):59-65 (May26, 2011) Inc., 2011
Age and Growth of Glossocardia obesa, a "Large" Bivalve in a Submarine
Cave Within a Coral Reef, as Revealed by Oxygen Isotope Analysis
AKIHISA KITAMURA
Institute ofGeosciences, Faculty ofScience, Shizuoka University, Shizuoka 422-8529, Japan
(e-mail: [email protected])
KEIGO TADA
Faculty of Environmental Earth Science, Hokkaido University, N10W5 Sapporo, 060-0810, Japan
SABURO SAKAI
Institute for Research on Earth Evolution, Japan Agency for Marine-Earth Science and Technology, Yokosuka
237-0061, Japan
NAGISA YAMAMOTO, TAKAO UBUKATA
Institute ofGeosciences, Faculty of Science, Shizuoka University, Shizuoka 422-8529, Japan
TSUZUMI MIYAJI
Department ofEarth and Planetary Science, University ofTokyo, Tokyo 113-0033, Japan
AND
TOMOKI KASE
National Science Museum, Tokyo, 169-0073, Japan
Abstract. Dark submarine caves are unique habitats from which most coastal species are excluded because of
darkness, marked oligotrophy, and reduced water circulation. Many bivalves have been found in caves oftropical
West Pacific coral reefs, but nearly all reported species are very small in adult shell size, generally <5 mm in length.
mm
Glossocardiaobesa(Reeve, 1843) isanexceptionallylargebivalvein thecavefaunaandgrows to 80 in adult shell
length. Since live specimens of G obesa are apparently very uncommon, there has been no study on its life-history
traits. We performed an oxygen isotope analysis ofa G. obesa (72 mm in shell length) collected alive in a submarine
caveatOkinawa Islands, Japan. The518 recordisdivided intoearly-and late-growthphases. Thereis no systematic
change in 818 valuein theearly-growthphase, whereas the 8lsO record for the late-growth phasecontains sixcycles.
Comparing the 8'80-derived temperatures from G. obesawith water-temperature records and 5lsO value ofseawater
G
in the cave shows that the 818 cycles of obesa reflect seasonal variation in water temperature. This result
demonstrates that the oxygen isotope analysis can usefully be employed to estimate growth and age in this species.
INTRODUCTION Kano et al., 2002; Motchurova-Dekova et al., 2002;
Kano & Kase, 2008; Ubukata et al., 2009). Kase &
Sheltered, submarinecavesdeveloped within coral reefs Hayami (1992) and Hayami & Kase (1993, 1996)
are inhabited by unique invertebrate communities that investigated cavernicolous bivalves from many caves in
include "living fossil" species and relatives ofdeep-sea Ryukyu Islands, Bonin Islands, Philippine Islands,
taxa (Jackson et al., 1971; Jackson & Winston, 1982; Saipan, Palau, and Guam, and reported >60 species,
Vermeij, 1987; Harmelin, 1997). Many workers have many of which share the following characteristics: (1)
addressed the ecological and evolutionary significance very small adult size (usually <5 mm in length); (2)
of the cryptic communities (Reitner & Gautret, 1996; unusually large prodissoconch I and an absence of
Page 60 The Veliger, Vol. 51, No. 2
prodissoconch II in many species, implying nonplank- dark inside, and deepens inward to its deepest point at
totrophic development; and (3) persistent denticles on 29 m below sea level. The floor iscovered by >1.4m of
the provinculum retained until the adult stage in many calcareous mud (Kitamura et al., 2007a). So-called
pteriomorph species, suggesting significant paedomor- living fossils, including the gastropod Neritopsis radula
phosis by progenesis. Kase & Hayami (1992) interpret- and the bivalve Pycnodonte taniguchii, have been found
ed these characteristics to indicate a relatively small alive in the cave (Hayami & Kase, 1992; Kase &
number of larvae and a predominantly K-selected Hayami, 1992). In addition, at least 36 species of
reproductive strategy. The authors regarded these cavernicolous microbivalves have been identified from
ecological features as adaptations to nutritional defi- the sediments of the cave (Kitamura et al., 2007a).
ciency in the submarine caves, as widely documented Kitamura et al. (2007b) measured water temperatures
by Fichez (1990, 1991). hourly in the cave from July 26, 2003 to July 6, 2004,
Although most ofthe bivalves in the caves are very documenting seasonal variation from 21°C (February)
small in adult shell size, the trapeziid Glossocardia to 29°C (late August to early September; Figure 2A).
obesa, a shallow infaunal suspension feeder, is an
exceptionally large bivalve in the cave fauna (Hayami METHODS
& Kase, 1993). Shell length exceeds 80mmandthe shell
volume is over X2000 greater than those of other Water samples for oxygen isotope analyses were
cavernicolous microbivalves. Hayami & Kase (1992, collected within Daidokutsu and upon the reef slope
1996) reported that the soft part of G. obesa is much at 30-m depth on July 2, 2007 (10:50-11:15 a.m. Japan
tshmeailrlesroftthabnodtiheast eaxrpeecsttieldl fmourcthheilrarsgheelrltshizaen; htohwoesveero,f t(Sim18eO;wF)igwuerree1u).ndOexrytgaekennisatototphee aGneaol-ySsceiseMnoAcfeTthLeabwoartae-r
tory in Nagoya, Japan, using a Finnigan delta S.
other cavernicolous microbivalves. 5,8Ow ratios are reported relative to Vienna Standard
This species, distributed in the tropical West Pacific Mean Ocean Water (V-SMOW), and the analytical
region, lives in both the open sea and cryptic
environments such as submarine caves developed precision (1 SD) was better than ±0.1%o. Salinity and
within coral reefs (Matsukuma & Habe, 1995). Morton temperature were measured using a temperature-
salinity meter at the time ofcollecting water samples.
(1979) described this bivalve as a deepwater species, The specimen of G obesa was embedded directly in
and it has also been recorded in shelly gravel bottoms polyesterresin without anychemical treatment, and cut
at between 5- and 60-m water depth (Okutani, 2000). along the axis of maximum growth. The section was
However, there has been no study of the life-history
traits of G. obesa because it is very rare to encounter pgorwoduenrd,wiatnhd 1p2h0o0tosigcragrpiht,edpoulnisdheerd twriatnhsm3i-ttuemdAl1i2ght.3
living individuals in either the open sea or cryptic
Powdered carbonate samples were collected from the
environments such as submarine caves.
outershell layerusingan automated Micromill sampler
In this paper, we examined the pattern and rate of
at the Japan Agency for Marine-Earth Science and
shell growth ofa single specimen of G. obesa collected Technology (JAMSTEC), Japan (Sakai, 2007). The
alive in a submarine cave developed within a coral reef width ofthe sample grooves was 2 mm (80-120 mg in
(Figure 1), from the perspective of oxygen isotope weight) from the umbo down to 52 mm, and the width
plrioffei-lheiss.toTrhyitsramietsthoofdliisvicnogmamnodnleyxtuinscetdbtiovdaelcviephseperctihees was 1 mm (50-70 mg in weight) from the 52-mm point
(e.g., Jones et al., 1983, 1986; Tanabe & Oba, 1988; troecethievedshenlol maadrdgiitnio.naTlhethpeorwmadleroerdcchaermbiocnaaltetrseaamtpmleenst
Goodwin et al., 2001; Schone et al., 2003; Watanabe et prior to oxygen isotope analysis. The sample was
al., 2004). The proportion of different isotopes of
analyzed using a mass spectrometer (IsoPrime, Micro-
oxygen present in the shell carbonate reflects the mass) at JAMSTEC. Individual samples were reacted
ambient water temperature in which the shell was with 100% phosphoric acid at 90°C Oxygen isotope
dt,seeOpmopisesirotatetoduprebeeisscapruerlesacetiipivinetlacytoelmddoerirnetwoaotftheterhesmheollirlg,ehtweohrfiliteehOeathihseioagtvhoipeeerr PvaeleuDeeseofbeslheelmlnictaer,boannadteth(5e18aOnacl)yatriecarlepporretceisdiroenla(t1ivSeDt)o
was better than ±0.1%o. X-ray diffractometer analysis
is precipitated.
revealed that the shell of G. obesa consists entirely of
aragonite.
SHELL DESCRIPTION and STUDY AREA
RESULTS
We
obtained a shell of G. obesa collected alive by a
scuba diver in the submarine Daidokutsu cave located There is no significant difference in both salinity and
in the northeastern coast ofIe Island, Okinawa Island 818Ow between inside the cave and at 29-m depth
(Figure 1), in early August 2004. The cave's entrance (Table 1). The 518Ow-salinity relation is similar to the
lies about 19 m below sea level. The cave is 40 m long, linear relationship proposed by Oba (1988) for surface
'
A. Kitamura et al., 2011 Page 61
B
28°N
^T^Tr^\
/£- .^Daidokutsu
le Island || n>>+* cave
lo
Okinawa »\V\\ I II.! I!.—III./Pil 1Jf/\) \*
—J J<7T H^ L— *
Island
'
le Island 1 reef ereSt
Pacific Ocean Pleistocene Ryukyu limestone
24°N
124°E 130°E 5km
I pre-Tertiary , 1
i 1
vertical section
sw
reef flat reef crest low tide
Daidokutsu cave 19 m depth
sample
live
5m
sediments
-29 m depth water sampling points
Figure 1. Locality map showing sampling site for Glossocardia obesa and Daidokutsu cave.
water extending from the East China Sea to the These six cycles are subdivided into four earlier cycles
Kuroshio Current off the southern Japanese Islands, (1—4) and two latercycles (5 and 6). The 518Oc values in
which is 5,8Ow = 0.203 S - 6.76 (S = salinity). the former range from —2.6 to —0.8%o, while in the
Seven translucent growth lines with widths of 0.9- latter from —2.0 to —1.2%o. There are two translucent
mm
1.3 were observed in the outer shell layer under growth lines in Cycle 1, but only a single growth line
transmittedlight (Figure 3). The 518Ocrecordisdivided was observed in each of the later cycles. These lines
into early- and late-growth stages at a point located correspond to light oxygen isotope values in each cycle
about 34 mm from the umbo (Figure 3). The early- (Figure 3). There are anomalously high 8I8Oc values at
growth stage shows no systematic variation in 818Oc a point located 26 mm from the umbo and at the shell
values, which range from —1.8 to 0%o. In contrast, the margin. Such exceptionally heavy 518Oc values were
518Oc record for the late-growth stage contains six often reported from other bivalves, such as Mesodesma
cycles (Cycles 1 to 6; Figure 3) for which the donacium (Carre et al., 2005), but their origin remains
wavelength decreases with distance from the umbo. poorly understood.
.
Page 62 The Veliger, Vol. 51, No. 2
—
— observed temperatureswithin the cave
A mean monthly watertemperature at 30 m depth
2003/7/27-2004/6/27 watertemperature
35.0
34.5
Figure 2. A, Comparison ofobserved temperatures with mean monthly water temperature at 29-m depth (the JODC). Data of
observed temperatureswithinthecavearefrom Kitamuraetal. (2007b); B, Seasonal variations in salinity at 29-mdepth. Data are
sourced from database compiled by the JODC. Error bars ofmonthly temperature and salinity represent standard deviation (Ict)
from monthly value for the period between 1906 and 2003.
DISCUSSION Water temperatures were calculated using the
equation ofCarre et al. (2005):
It is generally accepted that the oxygen isotopic
composition of bivalves is influenced by the tempera- r(°C)=(17.41+1.15)
ture and isotopic composition ofthe ambient seawater
in which the animal formed its shell. As noted above, -(3.66±0.16)(<S18Oargonite-<518Ow)
5In18Oadwdiitniotnh,etchaevereilsateiqounaslhitpobtehtawteaetn25918-Omwwaatnedrsdaleipntiht.y 5Ex18cOep-tdefroirvedtwotemexpceerpattiuorneasllybahseeadvyu5p1o8n vuasliunegs, tahlel
tifonhrsaein,desteahaanstdonpoaruletvsviiaodrueisatlthyieopncraiovnpeo8is1s8eOndowtbwyciotOnhsbiinadet(rh1ae9b8cl8ay)v.deifTcfhaeenrrebene-t vteaqerumiapatectirioaontnuirnoef5r18aC0na-grdereeriinveettdhetaelc.mapvee(r2a0(t0Fu5ir)geurifeselc4la)..w8Ti1thh%eino6f.5ttChhCee
estimated using salinity data at 30-m depth (S30m), as annual range oftemperatures in the cave from July 26,
compiled 1byX1th°e Japan Oceanographic Data Center 2003 to July 6, 2004 (8°C). We therefore consider that
2l(0oJ0nO1gD)i,Ctu;daend127t-h1e28°agEbr,oidvedactela5ls,8,Ofrwloa-mtsiatluitdnheiety2pe6rr-ei2lo7ad°tiNo1n8sa7hn4id-p tt5heemapne5dr18aO6tucmracey.yclTrehesfelreercfetlleaacttidvesecleryaessaomsnaealllinfalsmupaclmtiputaltuiidnoegnssroeifsnoClwyuacttlieeosrn
(Oba, 1988). due to a slowdown or cessation in shell growth. The
suBmamseerdtoon3t4h.e8diantwaionfteJrO(DFCig,urSe302mB)r.anWgeesrfergoamrd3e4d.5thien prreolfaitlieosnsihnidpicbaettewseethnattratnhselsuecelnintesgrwoewrtehflionremseadnddu5r1i8Ongc
8l8Ow value in the cave for the entire year to be 0.3 ± warm seasons (Figures 3, 4). This interpretation is
0.03%o ifthe 818Ow-salinity relationship is adopted. consistent with the fact that the shell margin (i.e., the
most recently formed shell material) of the study
specimen collected in early August 2004 is not
Table translucent. If this relationship is assumed, the last
1
translucent growth line (Cycle 6) is supposed to have
Oxygen isotope values obtained for water sampled been formed during the warm season of 2003. This
from within Daidokutsu cave and upon the reef slope result demonstrates that oxygen isotope analysis
off Ie Island, Okinawa, Japan. Locations of sampling appears to work well for this species and has the
points are shown in Figure 1. potential to provide useful growth and age estimates.
We analyzed the pattern ofthe growth curve ofshell
Area Reefslope Daidokutsu
length against annual growth lines (translucent growth
Depth (m) 10 20 30 29 lines) in the specimen based on the number ofseasonal
TSaelmipneitryature (°C) 2393..24 2338..10 3273..52 2364..62 2354..32 cycles of 8'8Oc (Figure 5). A series of measured data
518Ow(%„;vs. V-SMOW) 0.4 0.3 was approximated by thevon Bertalanffyequation and
a best-fit curve to the data was numerically calculated
1
A. Kitamura et al., 201 Page 63
1999 2000 01 02 03
20 30 40 50 60
Distance from umbo (mm)
Figure 3. A, Exterior of left valve; B, Optical transmitted-light photograph of the longitudinal shell section. Arrows show
translucentgrowthlines;C,OxygenisotopicprofileforourspecimenofGlossocardiaobesa. Verticalgraybarsrepresentthelocation
oftranslucent growth lines. Numbers 1-6 are inferred to be cycles bounded by neighboring troughs.
with a least-squares method. Because a seasonal cycle Case II ratherthan that ofCase I (Figure 5). The result
of 8l8Oc was unclear in the early-growth stage, we suggests that the bivalve started to form annual lines in
assumed the following two cases for regression the second summer or later and lived for at least 8 yr
analyses: (1) the bivalve regularly formed each annual until 2003 (Figure 4).
growth line in every summer through which the shell Combining oxygen isotope analysis with an analysis
has passed (Case I), and (2) the animal failed to form of absolute growth pattern allow us a reasonable
one or a few distinct annual lines in the early-growth estimation of age and life-history traits of G. obesa.
stage (Case II). In.Case I, the first translucent growth Studies on the life-history strategy of this species may
line is supposed to have been formed within 1 yr after provide a clue to reveal the reason why such a "huge"
hatching. In this case, the beak point with shell length bivalve is a constituent of the refugial community
mm
of was regarded as the "zeroth" annual dominated by microshells.
increment and the plot of(0,0) was used together with
biometric data for regression analysis. On the other
hunatnidl,thifewfierstasasnunmuealCagsreowItIh, iltinteowoakslofnogremredthaannd1thyer AKictkanzoawtloe.dgWmeentasl.soWtehagnrakteKfu.llYyaascukmnuowrlaedfgoeraadsvsiicsetsanfcreomwiHt.h
sample collection. This study was funded by Grants-in-Aid
"zeroth" annual increment does not represent the start 16340159 and 19540492 awarded by the Japan Society for
ofthe shellgrowth. In thelattercase, therefore, theplot Promotion ofScience, the Japan Science Society, a Sasakawa
of(0,0)wasnot used forregressionanalysis. Thefitness Scientific Research Grant, and a Grants-in-Aid from the
ofobserved data to the von Bertalanffy curve supports Fukada Geological Institute.
Page 64 The Veliger, Vol. 51, No. 2
1997 1998 1999 2000 01 02 03
30 40 50 60
Distance from umbo (mm)
maximum temperature in Daidokutsu cave
minimum temperature in Daidokutsu cave
Figure 4. Reconstructed temperature record based on shell oxygen isotope data using the equation ofCarre et al. (2005).
80 80
Case Case
I
I t <
^+~
60 " 60
o) 40 g>40
CD
CD
CO 20 -7 L = 67.2(1-g-0.91f+0.9\ co 20 h /_ = 74.2(1-e-038f-052)
r ~ 0.9946 r = 0.9996
l
12 • x12 a.
3 4 5 3 4 5 6
Annual increment number Annual increment number
Figure5. Predictedvon Bertalanffygrowthcurvesestimatedinthetwocases: I,thefirstannualgrowthlinewasformedinthefirst
summer; or II, it was recorded in the second summer or later.
A. Kitamura et al., 2011 Page 65
LITERATURE CITED Kase, T. &I. Hayami. 1992. Unique submarinecavemollusc
fauna: composition, origin and adaptation. Journal of
Carre, M., I. Bentaleb, D. Blamart, N. Ogle, F. Molluscan Studies 58:446-449.
Cardenas, S. Zevallos, R. M. Kalin, L. Ortlieb & Kitamura, A., M. Hiramoto, T. Kase, N. Yamamoto, M.
M. FONTUGNE. 2005. Stable isotopes and sclerochronol- Amemiya & S. Ohashi. 2007a. Changes incavernicolous
ogy of the bivalve Mesodesma donacium: potential bivalveassemblagesandenvironmentswithinasubmarine
application to Peruvian paleoceanographic reconstruc- cave in Okinawa Islands during the last 5000 years.
tions. Palaeogeography, Palaeoclimatology, Palaeoecol-
Paleontological Research 11:161-180.
Fichoegzy, 2R2.8:149-9205..Decrease in allochthonous organicinputs in KitaHmiurraam,otAo.,, HN..FYuakmuasmaowta,o,T.TW.aKtaasnea,beS,. TO.haIsrhiino,,MH..
dbeanrtkhicsucbommamruinnietycarviecsh,nescso.nnHeycdtrioobniolwoigtiha 2l0o7w:e6r1i-n6g9.in Kojitani, M. Shimamura & I. Kawakami. 2007b.
Potential of submarine-cave sediments and oxygen
Fichez, R. 1991. Suspended particulate organic matter in a
Mediterranean submarine cave. Marine Biology 108:167- isotope composition of cavernicolous microbivalve as a
late Holocene paleoenvironmental record. Global and
174.
GoodDweitnt,maDn.. H2.0,01.K.CrWos.s-Fcalleisbsraa,tioBn. oRf.daSiclyhOgnreowt&hDi.ncrLe.- MatsPluaknuetmaar,y CAh.an&geT.55:H3a0b1e-.3161.995. Systematic revision of
ments,stableisotopevariations,andtemperatureintheGulf living species ofMeiocardia, Glossidae and Glossocardia,
ofCalifornia bivalve mollusk Chione cortezi: implications Trapezidae (Bivalvia). Memoires du Museum national
forpaleoenvironmental analysis. Palaios 16:387-398. d'Histoire naturelle 167:75-106.
Harmelin, J. G. 1997. Diversity of bryozoans in a Morton, B. 1979. Someaspectsofthebiologyandfunctional
Mediterranean sublittoral cave with bathyal-like condi- morphology of Trapezium (Neotrapezium) sublaevigatum
tions: role ofdispersalprocessesand localfactors. Marine (Lamarck) (Bivalvia: Arcticacea). Pacific Science 33:177—
Ecology Progress Series 153:139-152. 198.
Hayami, I. & T. Kase. 1992. A new cryptic species of Motchurova-Dekova, N., M. Saito& K. Endo. 2002.The
Pycnodonte from Ryukyu Islands: a living fossil oyster. recent rhynchonellide brachiopod Parasphenarina caver-
Transactions and Proceedings of the Palaeontological nicola gen. et sp. nov. from the submarine caves of
Society ofJapan, New Series 165:1070-1089. Okinawa, Japan. Paleontological Research 6:299-319.
Hayami, I. & T. Kase. 1993. Submarine cave Bivalvia from Oba, T. 1988. Paleoceanographic information obtained bythe
the Ryukyu Islands: systematics and evolutionary signif- isotopic measurement of individual foraminiferal speci-
icance. The University Museum, The University ofTokyo, mens. Pp. 169-180 in Proceedings of the First Interna-
Bulletin 35:1-133. tional Conference on Asian Marine Geology. China
Hayami, I. & T. Kase. 1996. Characteristics of submarine Ocean Press: Beijing.
cave bivalves in the northwestern Pacific. American Okutani, T. (ed.). 2000. Marine Mollusks in Japan. Tokai
Malacological Bulletin 12:59-65. University Press: Tokyo. 1173 pp.
Jackson, J. B. C, T. F. Goreau & W. D. Hartman. 1971. Reitner, J. & P. Gautret. 1996. Skeletal formation in the
Recent brachiopod-coralline sponge communities and modern but ultraconservative chaetetid sponge Spiras-
their paleoecological significance. Science 173:623-625. trella (Acanthochaetetes) wellsi(Demospongiae, Porifera).
Jackson, J. B. C. & J. E. Winston. 1982. Ecology ofcryptic Facies 34:193-208.
coralreefcommunities. 1. Distribution and abundance of Sakai, S. 2007. High-precision micro-milling system. IFREE
major groups of encrusting organisms. Journal of Ex- Report for 2005-2006, Technology, Part 1:65-67.
JapapneriOmceenatanlogMraraipnheicBioDlaotgyaaCnedntEecorl.og2y00577.:1J3O5-D1C47.Data SchoEnnev,irBo.nRm.e,ntKa.lTcaonnatbroel,sDo.nLs.heDllegtrtomwathnr&ateS.sSaantdo.8ls2O003o.f
On-line Service System, http://www.jodc.go.jp/service_j. theshallow-marinebivalvemollusk Phacosomajaponicum
Jonehst,m.D.AccS.e,ssDe.d MF.arWcihll1,ia20m0s9.& M. A. Arthur. 1983. TanaibneJ,apKa.n.&MaTr.inOebaB.iol1o9g88y.14La2t:i4t7u3d^i4n8a5l.variation in shell
Growth history and ecology of the Atlantic surf clam
growth patterns of Phacosoma japonicum (Bivalvia:
Spisulasolidissima(Dillwyn)asrevealedbystableisotopes Veneridae) from the Japanese coast. Marine Ecology 47:
and annual growth increments. Journal of Experimental
75-82.
JonehsMi,asrtDio.nryeS.,BoifDo.lsoFyg.mybWaiionlndlt-iEbcaeomalsroig&nygC7.3g:iS2a.2nt5R-o2cm4l2aa.nmesk.fro19m86.stLaibflee Ubuk2a00t9a.,AT5.,000A-.yeKairtfaosmsuilrrae,coMrd.ofHilarravamlostheoll&morTp.hoKlaoseg.y
ofsubmarine cave microshells. Evolution 63:295-300.
isotope profiles. Science 231:46-48. G
Kano, Y., S. Chiba & T. Kase. 2002. Major adaptive Vermeij, J. 1987. Evolution and Escalation: an Ecological
radiation in neritopsine gastropods estimated from 28S History of Life. Princeton University Press: Princeton,
2rR6oR9yN:a2Al45S7so-ec2qi4ue6et5nyc.eosfaLnodndfoonss.ilSerreiceosrdsB., PBiroolcoegeidcianlgsScoiefnctehes WataNOngeaawbweJae,.rsTe2.y0,.04A5..27ASpupz.6u0k-iy,earH.isKotaowpiachartecao,rdH.froKmana &midS-.
Kano, Y. &T. Kase. 2008. Diversityand distributionsofthe Holocenefossilgiantclam(Tridacnagigas) inthe Ryukyu
submarine-cave Neritiliidae in the Indo-Pacific (Gastro- Islands: physiological and paleoclimatic implications.
poda: Neritimorpha). Organisms, Diversity & Evolution Palaeogeography, Palaeoclimatology, Palaeoecology 212:
8:22^13. 343-354.