Palaeogeography, Palaeoclimatology, Palaeoecology 292 (2010) 443–452

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Palaeogeography, Palaeoclimatology, Palaeoecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e oReconstruction of light conditions within a submarine cave during the past
7000 years based on the temporal and spatial distribution of algal symbiont-bearing
large benthic foraminifers
A. Omori a, A. Kitamura a,⁎, K. Fujita b, K. Honda b, N. Yamamoto aabInstitute of Geosciences, Faculty of Science, Shizuoka University, Shizuoka 422-8529, Japan
Department of Physics and Earth Sciences, University of the Ryukyus, Okinawa 903-0213, Japana r t i c l e

i n f oArticle history:
Received 27 December 2009
Received in revised form 24 March 2010
Accepted 8 April 2010
Available online 14 April 2010
Keywords:
Algal symbiont-bearing large benthic
foraminifer
Cavernicolous bivalves
Submarine cave
Light conditionsa b s t r a c t
Coral reef cavities, crevasses, and caves are inhabited by cryptic communities. The sediments within thesubmarine Daidokutsu Cave (29 m water depth) on the fore-reef slope of Ie Island, Okinawa, Japan, preservea fossil record of cryptic bivalve species over the past 7000 years. The record suggests that inﬁlling of cavities
caused a progressive decrease in the exchange of water between the interior and exterior of the cave,
resulting in a decline in food supply to the cave. To test this hypothesis, the light conditions within the cavewere reconstructed from the spatial and temporal distributions of algal symbiont-bearing large benthic
foraminifers, based on the assumption that inﬁlling of reef cavities would have resulted in reduced lightintensity within the cave. The results show that progressive darkening of the cave occurred by about 5130 yr
BP, synchronous with a weakening in water ﬂow within the cave. This synchronicity indicates that inﬁlling ofcavities and narrowing of the cave entrance might cause declines in the exchange of water between theinterior and exterior of the cave, as well as in light intensity within the cave. These resulted in a deﬁciency infood in the cave, thereby affecting the species composition of cavernicolous bivalves.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction
Cavities and caves are estimated to constitute between 60% and
75% of the total available surface of a coral reef (Jackson et al., 1971;
Buss and Jackson, 1979; Logan et al., 1984) and between 30% and 75%of the bulk volume (Garrett et al., 1971; Ginsburg, 1983; Kobluk andvan Soest, 1989). Such spaces are occupied by unique invertebrate
communities (Jackson et al., 1971). Many workers have investigatedthe ecological and evolutionary signiﬁcance of such communities(Jackson and Winston, 1982; Kobluk, 1988; Reitner and Gautret,
1996; Wörheide, 1998; Tabuki and Hanai, 1999; Kano and Kase, 2000;
Kano et al., 2002; Kase and Kano, 2002; Ubukata et al., 2009) andseasonal to annual changes in environmental conditions within reef
cavities (Gili et al., 1986; Fichez, 1990a,b, 1991; Harmelin, 1997;
Lejeusne and Chevaldonné, 2005). In addition, several studies haveexamined the ﬂuxes of various materials (e.g., dissolved oxygen,dissolved inorganic matter, dissolved organic matter, and bacterioplankton) in reef cavities (e.g., Ayukai, 1995; Yahel et al., 1998; Van
Duyl et al., 2002; Scheffers et al., 2004; Van Duyl et al., 2002, 2006).
For example, de Goeij and Van Duyl (2007) documented that coralcavities are a sink of dissolved organic carbon (DOC) which is⁎ Corresponding author.
E-mail address: seakita@ipc.shizuoka.ac.jp (A. Kitamura).
0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2010.04.004

produced by reefs and reef overlying waters, and possibly supplied
from land-based sources. According to de Goeij et al. (2008),
encrusting cryptic sponges are of quantitative importance in theremoval of DOC in coral reef cavities.
Hayami and Kase (1992, 1993, 1996) and Kase and Hayami (1992)
reported about 60 species of cavernicolous bivalves in tropical westPaciﬁc coral reefs, including Daidokutsu Cave, which is the focus of thepresent report. Most species are epifaunal or semi-infaunal suspension feeders, with no photosymbiotic or chemosymbiotic species
being reported. However, no previous studies have investigatedmillennia-scale variations in the community of these organisms ortheir environment, with the exception of Kitamura et al. (2007a) andYamamoto et al. (2009).
Kitamura et al. (2007a) examined the species composition of
cavernicolous bivalves from the surface and two sediment cores(Cores 04 and 06) within Daidokutsu Cave of Ie Island, northwest of
the main island of Okinawa, Japan (Figs. 1 and 2). The results showedthat species living in the innermost area of the cave (the 1st group)
became dominant in the past 5000 yr, whereas species living near the
cave entrance (the 2nd group) declined in abundance during this time
(Figs. 3 and 4). This ﬁnding indicates that the environmental
conditions typically seen in the innermost cave area gradually spread
across the cave. It is well known that the number of species andbiomass show a progressive reduction toward the cave interior (e.g.,
Harmelin et al., 1985; Gili et al., 1986). This pattern has been

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Fig. 1. Location map of the submarine Daidokutsu Cave on Ie Island, west of Motobu Peninsula, Okinawa Island, Japan (A, B), and simpliﬁed transverse section through the cave (C).

explained by a decrease in the amount of organic matters provided bywater ﬂow from the open sea into the cave, with increasing distancefrom the cave entrance (Gili et al., 1986; Fichez, 1990a,b, 1991;
Harmelin, 1997). Thus, Kitamura et al. (2007a) concluded that in thecase of Daidokutsu Cave, faunal changes in the bivalve assemblage
suggest a gradual increase in extent, over the past 5000 yr or more, of
the cave area deﬁcient in foods. In addition, the authors interpreted
that the inﬁlling of cavities had led to reduced exchange of water
between the interior and exterior of the cave, resulting in a
progressive decline in food supply.
Yamamoto et al. (2009) extended the record of the distribution ofbivalves and sediment within Daidokutsu Cave up to 7000 years BP,
based on an analysis of a sediment core (Core 19; Fig. 5). The authors
found brown sand-sized grains within sediments corresponding to
the period 7000–6000 cal BP, and identiﬁed them as debris derived

from a red soil layer formed in coastal zones around Ie Island.
Moreover, the authors showed that the decline in abundance of very
coarse sand-sized debris (1.0–2.0 mm in diameter; VCS debris)
preceded that of coarse sand-sized debris (0.5–1.0 mm in diameter;
CS debris) by about 550 years (Fig. 5), and regarded this difference as
direct evidence of a weakening in water ﬂow within the cave. The
disappearance of VCS debris at about 6500 cal BP was not accompanied by a change in bivalve assemblage, although the observed
expansion of the 1st group coincided with the termination of CS
debris at about 6000 cal BP. Thus, an examination of the cause of thetermination of CS debris would provide information that could be
used to test the validity of Kitamura et al.'s (2007a) hypothesis thatmillennia-scale variations in cavernicolous bivalve assemblages werestrongly inﬂuenced by a decline in food supply associated with the
inﬁlling of reef cavities.

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445

Fig. 2. Bathymetric map showing the locations of sampling points for surface sediments (a–f, 1) and cored sediments. Also shown is the distribution of surface sediment facies (seetext for details).

However, there are two possible explanations of the termination of
CS debris. The ﬁrst interpretation assumes that the development ofreef ﬂats protected the coastal zones and thereby prevented erosion
and transport of the red soil layer by high wave energy (Neumann,
1972; Hopley, 1984; Montaggioni, 2005). A second interpretation
assumes that the inﬁlling of cavities and narrowing of the caveentrance resulted in reduced water ﬂow within the cave.
To evaluate the above interpretations, this study reconstructedtemporal trends in light conditions within Daidokutsu Cave based on an
analysis of the distributions of algal symbiont-bearing large benthic
foraminifers (LBF) recovered from the surface and cored sediments
within the cave. With inﬁlling of the cavities and narrowing of theentrance, the interior of the cave would have become progressively
darker. Distributions of living algal symbiont-bearing LBF are mainly
controlled by temperature, light, water motions, substrate types, andnutrient levels (Hallock, 1999; Hohenegger, 2004; Renema, 2006;
Uthicke et al., 2010). Of these parameters, light is the most importantfactor affecting depth distributions of algal symbiont-bearing LBF (e.g.,
Hallock, 1999; Hohenegger, 2004). Previous studies have provided a

detailed account of the depth distribution of LBF around Sesoko Island,
which is located 10 km southeast of Ie Island (Fig. 1; Hohenegger, 1994;
Hohenegger et al., 1999; Yordanova and Hohenegger, 2002). This
database in the same physico-chemical oceanographic setting enables
us to reconstruct the light conditions within the cave.
Although many studies have examined the species compositions ofbenthic foraminifers within littoral and anchialine caves (Denitto
et al., 2007; van Hengstum et al., 2008, 2009a,b), we are unaware ofany published studies that have searched for millennia-scale variations in the species composition of LBF in completely submergedmarine caves. This study is the ﬁrst to describe the taxonomic
composition and temporal–spatial distribution of algal symbiontbearing LBF in submarine caves.
2. Study area
Daidokutsu Cave is located on the northeastern coast of Ie Island,
Okinawa, Ryukyu Island Arc (Fig. 1A, B). The cave's entrance lies inabout 19 m water depth on the fore-reef slope, and is roughly 18 m

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A. Omori et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 292 (2010) 443–452

Fig. 3. Spatial distributions of selected cavernicolous bivalve species in Daidokutsu cave (modiﬁed after Yamamoto et al., 2009). Percentages are given relative to the total number ofindividuals of all bivalve species. The locations of sites a–f are shown in Fig. 2.

wide and 2 m high. The interior of the cave is very dark, 40 m long,and deepens abruptly inward to a maximum depth of 29 m (Fig. 1C).
The ﬂoor near the cave entrance is covered with cobbles and boulders,
while the ﬂoor of the interior is covered by calcareous sand and mud(Fig. 2). Kitamura et al. (2007a) divided the surface sediments in theinterior into three facies (Fig. 2); Facies 1 is gray calcareous sand that
occurs close to the entrance, Facies 2 is gray calcareous mud that
occurs in the inner part of the cave, and Facies 3 is calcareous sandcontaining the skeletons of partly encrusted coralline sponges, which
occurs in patches within Facies 2.
Water temperature inside the cave ranges from 29 °C (August) to
21 °C (February), showing similar seasonal variations to that observed
at 30 m depth in the open sea around Okinawa (Kitamura et al.,2007b; Kitamura and Yamamoto, 2009). If we accept the sea-level
curve proposed by Fairbanks (1989), Bard et al. (1996), and Toscanoand Macintyre (2003), the cave was possibly completely submerged

Fig. 4. Columnar sections of submarine-cave sediment within Core 06, showing stratigraphic changes in lithology and carbonate content, and abundances of debris, dominant large
benthic foraminifer species and cavernicolous bivalve species, along with depositional rates inferred from the 14C ages of molluscs (modiﬁed after Yamamoto et al., 2009).

A. Omori et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 292 (2010) 443–452
Fig. 5. Columnar sections of submarine-cave sediment within Core 19, showing stratigraphic changes in lithology, carbonate and mud contents and abundances of debris, dominant large benthic foraminifer species, and cavernicolous bivalve
species, along with depositional rates inferred from the 14C ages of molluscs (modiﬁed after Yamamoto et al., 2009).

447

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by about 8000 yr BP. Sea level has remained at its present height
during the past 7000 yr (Montaggioni, 2005).
3. Materials
3.1. Sediments from the cave ﬂoor and reef slope
Kitamura et al. (2007a) examined the cavernicolous bivalve
assemblage in surface sediments (uppermost 5 cm) collected at six
sites within Daidokutsu Cave (a–f; Fig. 2). In the present study, we
documented the LBF assemblage in these samples, as well as in theuppermost 5 cm of cored sediments (Core 04) collected from theinnermost cave area (Fig. 2). For comparison, we also analyzed the LBF
assemblage in a surface sediment sample collected from the reef slope(46.2 m below sea level; Fig. 1) and a living LBF assemblage in thesurface sediment sample (70 g in weight) from site 1, which was
located close to site b (Fig. 2).
The cavernicolous bivalves Cosa kinjoi and Parvamussium crypticum(1st group) are found within surface sediments at three sites (d–f) in the
innermost cave area, while Cosa waikikia and Hiatella sp. aff. H. orientalis(2nd group) are observed within surface sediments at four sites (a–d)
near the cave entrance (Kitamura et al., 2007a) (Fig. 3). According toYamamoto et al. (2009), a very small amount of debris (less than one
grain per 12.5 g) from the red soil layer is recognized in surface
sediments at three sites in the cave (d–f), but is not found in surface
sediments at the other three sites (a–c) in the cave and on the reef slope.
3.2. Cored sediments
As noted above, Kitamura et al. (2007a) and Yamamoto et al.
(2009) investigated temporal changes in the cavernicolous bivalve
assemblage within three sediment cores. In the present study, we
examined the LBF assemblage in Cores 06 and 19.
Core 06 (148 cm length) can be divided into a lower part, consistingof yellow calcareous mud (N22 cm length), and an upper part consistingof gray calcareous mud (approximately 126 cm length) (Kitamura et al.,2007a) (Fig. 4). The sharp boundary between the two parts is estimatedto represent an age of about 5450 cal BP. The gray calcareous mud isinterpreted to have been deposited continuously at a sedimentation rateof ca. 21.1 cm/kyr. The 14C ages of samples obtained from the lower partof the core fall within a narrow range from 5980 to 5060 cal BP, showing
a non-linear relationship with depth (Fig. 4). Accordingly, Kitamura
et al. (2007a) considered the possibility that the sediment in the lower
part originated as a sediment gravity ﬂow. CS debris occurs sporadicallyin Core 06, while VCS debris is not found (Fig. 4). Molluscs of the 1stgroup show a rapid increase in abundance immediately above theboundary between the yellow and gray calcareous muds. The species ofthe 2nd mollusc group show a decrease in abundance at about 2200 cal
BP.
Core 19 preserves a record of fossils and sedimentation over the
past 7000 years (Yamamoto et al., 2009). The sediment in the coreshows a ﬁning-upward trend, and is divided into an underlying graycalcareous sand (233–178 cm depth) and an overlying gray calcareous mud (178–0 cm depth) (Fig. 5). The sedimentation rate isestimated to be 41.7 cm/kyr between 233 and 153 cm depth, and28.9 cm/kyr between 153 and 0 cm depth (Fig. 5). The VCS debris
from the red soil layer is only found in the lower part of Core 19(Fig. 5), and the abundance of the debris (the number of grains pergram of sediment) decreases upward from 0.6/g at 233 cm depth tob0.1/g at 203 cm depth. The abundance of CS debris decreases upwardfrom 10/g at 233 cm depth to b1/g at 180 cm depth. Two species of
the 1st mollusc group (Cosa kinjoi and Parvamussium crypticum) occur
almost continuously after the termination of CS debris at about
6000 cal BP (Fig. 5), while two species of the 2nd mollusc group (Cosawaikikia and Hiatella sp. aff. H. orientalis) show an upward decrease inabundance from about 72 cm depth.

4. Methods
Foraminifer tests were picked from the N0.5 mm size-fraction of
surface and cored sediment samples. For Core 06, we analyzed
foraminifer tests from samples collected at 1 cm intervals. The surface
sediment sample from site 1 was stained with a rose Bengal solution(1 g L− 1 of water), washed three times to remove surplus stain, anddried at 60 °C. From N0.5-mm size fraction of the residue, all stained
foraminiferal specimens with well-preserved test surfaces wereidentiﬁed as alive when collected, and isolated.
Foraminifer tests were identiﬁed to the lowest taxonomic level
and the number of individuals was counted for each taxon. Taxonomic
identiﬁcations were based on Hatta and Ujiié (1992a, b), Yordanova
and Hohenegger (2002), and Renema and Hohenegger (2005).
We calculated the relative abundance (%) of foraminifer species insurface sediment samples. The stratigraphic distribution of each species
in the cored sediments is expressed as abundance (the number of
specimens per gram of sediment) (Supplemental Tables 1 and 2).
To ﬁnd sediment sample groups with similar taxonomic composition, Q-mode cluster analysis was performed on log-transformed,
relative abundance data of foraminifer taxa using a group-average
linking method. For Cores 06 and 19, the top 25-most common taxa
were used for analysis, to exclude occurrence of rare species from thedata matrix. A Bray–Curtis dissimilarity coefﬁcient was used to
calculate a similarity matrix of taxonomic composition among
samples. The multivariate analysis and the Bray–Curtis dissimilarity
coefﬁcient were computed using the software PRIMER Ver. 5(PRIMER-E Ltd., England).
5. Results
A total of 61 taxa were identiﬁed from surface sediments in thesubmarine cave and on the fore-reef slope (Fig. 6; Table 1). Q-mode
cluster analysis demonstrated that living LBF assemblage was clearly
distinct from the dead assemblages in surface sediments (Supplemental Fig. 1). The dead assemblages could be divided into two
subassemblages. One subassemblage was found in the innermost cavearea (sites d–f, and Core 04). The sub-assemblage is dominated by
Amphistegina bicirculata, Calcarina mayori, Eponides repandus, Siphoniferoides siphonifera, and Rosalina petasiformis. Another subassemblage was found near the cave entrance and on the fore-reef slope(sites a–c, and fore-reef slope). The subassemblage was dominated by
Amphistegina lessonii, A. bicirculata, E. repandus, S. siphonifera, andPlanorbulina mediterranensis. Most symbiont-bearing species in thedead assemblages such as Amphistegina lobifera, A. lessonii, Heterostegina depressa, and Sorites orbiculus were found mainly near the caveentrance and the fore-reef slope, whereas A. bicirculata and C. mayori
occupied the innermost part of the cave (Fig. 7).
The living LBF assemblage in surface sediments from site 1 wasdominated by non-symbiotic E. repandus and Lenticulina spp. (Fig. 6;
Table 1). Many individuals of A. bicirculata and a few individuals of C.
mayori and H. depressa were found as living in surface sediments fromsite 1. We found no stained individuals of A. lessonii, A. lobifera, and S.
orbiculus.
A total of 38 and 78 taxa were identiﬁed from Cores 06 and 19,
respectively. LBF assemblages from the two cores were dominatedby Amphistegina bicirculata, E. repandus, Quinqueloculina lamarckiana, and S. siphonifera. Results of Q-mode cluster analysis demonstrated only one large cluster for the Core 06 data (Supplemental
Fig. 2), suggesting that LBF assemblages in the vicinity of Core 06
were generally stable over time. A. bicirculata was commonly foundthroughout Core 06, whereas A. lessonii, H. depressa, Calcarina
mayori, and Sorites orbiculus occurred sporadically (Fig. 4; Supplemental Table 1). We did not ﬁnd Amphistegina lobifera in Core 06. In
contrast, three major clusters could be recognized for the Core 19
data, being correlated to samples from the lower (149–233 cm),

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449

Fig. 6. Relative abundances of dominant benthic foraminifer species (those that make up N 3% of the total count in each sample; dead specimens except for site 1) in Daidokutsu Cave.
The locations of sites a–f, 1, Core 4, and the fore-reef samples are shown in Figs. 1 and 2.

middle (70–187 cm) and upper (0–135 cm) parts of the core
(Supplemental Fig. 3). A. lobifera, A. lessonii, H. depressa, and S.
orbiculus were commonly found in the lower part (233–151 cm
depth), but were rare in the upper 150 cm, which was deposited
after around 5130 cal BP (Fig. 5; Supplemental Table 2). Sorites
orbiculus was abundant within the horizon from 73 to 68 cm depth,
and C. mayori was relatively rare between 233 and 170 cm depth. A.
bicirculata showed a gradual increase in abundance between 233
and 210 cm depth, and was predominant throughout the interval
between 210 and 60 cm depth before showing a gradual upward
decrease in abundance from 60 cm depth.
6. Discussion
Large benthic foraminiferal assemblages from surface and coredsediments inside the cave are composed of diverse heterotrophic andalgal symbiont-bearing mixotrophic taxa. Algal symbiont-bearing
mixotrophic taxa are characterized by species adapted to hardsubstrates in a low-light condition (e.g., the deeper part of the euphotic
depths). It is notable that species adapted to soft (sandy) substrates in
the low-light condition such as Dendritina spp., Parasorites orbitolitoides,
Amphistegina radiata, Amphistegina papillosa, Nummulites venosus, andOperculina complanata (Hohenegger, 2004) were rare or absent. Thiswas possibly because of the lack of sandy area particularly in the innerpart of the cave and of relatively high-light conditions near the caveentrance.
In Core 19, Amphistegina lobifera, A. lessonii, H. depressa, and S.
orbiculus show a decrease in abundance from at least 7000 cal BP andoccur only sporadically after about 5130 cal BP, which corresponds tothe upper 150 cm in the core (Fig. 5). A. lobifera inhabits turf algaethat grow on high-energy reef crests throughout the Ryukyu Islands(Hohenegger, 1994; Iryu et al., 1995; Fujita, 2004), but rapidly
decreases in abundance down to 20 m water depth, and is not foundbelow 30 m depth (Hohenegger et al., 1999; Yordanova andHohenegger, 2002; Hohenegger, 2004). Therefore, favorable water
depths for this species are shallower than 15 m (Yordanova andHohenegger, 2002). The optimal conditions for A. lessonii are found inwater depths of 15–20 m with no substrate preference (Hohenegger,
2004; Renema, 2006): it is rare at the reef edge and is not found atwater depths exceeding 75–80 m (Yordanova and Hohenegger,
2002). The maximum abundance of S. orbiculus occurs on hardsubstrates (in particular, macroalgae; Hohenegger, 2004; Renema,2006) of reef slopes at 15 m depth; after a strong decrease inabundance down to 40 m depth, individuals are extremely rare at
50 m (Yordanova and Hohenegger, 2002).
Given that the present sea level has remained approximately
constant for the past 7000 years, the interior of Daidokutsu Cave
(29 m depth) during this period has been much darker than 30 m water
depth in the open sea. Therefore, there is no doubt that the interior ofcave has been an unsuitable environment for A. lobifera, A. lessonii, and S.
orbiculus. This is consistent with the absence of living individuals ofthese species from surface sediments at site 1 (Fig. 6; Table 1). However,many of their well-preserved empty tests occur in surface sediments
within the cave at sites near the entrance (sites a–c) (Fig. 7) as well as inCore 19 (Fig. 5). Since this preservational state indicates short transportdistances from the habitats of A. lobifera, A. lessonii, and S. orbiculus, these
species are interpreted to live on hard substrates of cobbles and walls
near the entrance of the cave at 19 m depth. Thus the upward decreasing
trend in A. lobifera, A. lessonii, and S. orbiculus within Core 19 is explainedby a decline in light intensity and/or weakening of water ﬂow within the
cave. The similar stratigraphic distributions of these species and CS
debris (Fig. 5) indicates that termination of the supply of debris wascaused mainly by a weakening of water ﬂow within the cave, rather thana reduction in sediment supply from paleosols and terrigenous
sediments deposited in coastal zones. Both S. orbiculus and CS debris
are abundant in the horizon from 73 to 68 cm depth, implying that
sediment reworking, although not signiﬁcant, occurred at about
2530 cal BP.
There exists a clear difference in the spatial and stratigraphic
distributions of H. depressa and C. mayori within Daidokutsu Cave. The
distribution of H. depressa is similar to that of A. lobifera, whereas the
distribution of C. mayori is similar to that of A. bicirculata in Core 19, asshown below (Figs. 5 and 7). The two species show similar
distributions around Sesoko Island (Yordanova and Hohenegger,
2002) as well as other area in the Ryukyus (Fujita, 2004), Indonesia(Renema, 2006) and inshore reefs of the Great Barrier Reef (Uthicke
et al., 2010). Heterstegina depressa is rare near the reef edge, but its
abundance shows a sudden increase at 10 m depth. The maximum

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Table 1
Census data of large benthic foraminifer species in surface sediments.
Species/site

Reef slope

Amphistegina bicirculata
Amphistegina lessonii
Amphistegina lobifera
Amphistegina papillosa
Amphistegina radiata
Amphistegina sp.
Anomalinella rostrata
Baculogypsina sphaerulata
Baculogypsinoides spinosus
Calcarina defrancii
Calcarina gaudichaudii
Calcarina hispida
Calcarina mayori
Calcarina sp.
Cibicides lobatulus
Cibicidoides sp.
Cribroeponides cribrorepandus
Cymbaloporetta squammosa
Cymbaroporetta tabellaeformis
Cymbaloporetta sp.
Elphidiidae
Eponides repandus
Glandulina ovula
Heterostegina depressa
Lenticulina spp.
Lingulinopsis sp.
Neoeponides sp.
Neorotalina calcar
Operculina ammonoides
Pegidia dubia
Planorbulinella larvata
Planorbulina mediterranensis
Planostegina operculinoides
Rosalina petasiformis
Sphaerogypsina globulus
Rotaliida
Amphisorus hemprichii
Dendritina sp.
Peneroplis pertusus
Peneroplis planatus
Peneroplis sp.
Pyrgo denticulata
Pyrgo sp.
Quinqueloculina bicarinata
Quinqueloculina lamarkiana
Quinqueloculina parkeri
Quniqueloculina rugosa
Quinqueloculina sp.
Sorites orbiculus
Spiroloculina sp.
Triloculina kerimbatica
Miliolida
Siphoniferoides siphonifera
Textularia agglutinans
Textularia crenata
Textularia dulpa
Textularia foliacea
Textulariida
Acervulinidae
Globigerinida
Spirillina ? sp.
Unidentiﬁed
Total

29
45
20
11
17
21
3
2
1
3
1
1
2
2
1

a

b
15
35
27
9
10
1
5
4
5
13
2
1
2
1

c

8
10
11
2
7
6
5
6
1
4
10
1

14
9
13

d

e

34

20

f

1

2
4
5
10

Core 0441
1
1

9

Stained individuals (site 1)
5

2
4
1

4
15

1

2
1

3

2
1

2

9

10

16

7

1
3
5

1
3
5

1

2

1
1
2
1

3

3

3

20

6
1
66

7
2
26

40

21

20
5

13
8

5
4

3
5

1

10

1

1
1

2
1

1
1

1
4
11
26
3

4

5
17
12
2
8
6
2

1
3
20
12
1
1
6
1
1

2

2
15
9
2
2
4
1
3

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92
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51
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2
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7
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1

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3
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319

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407

6
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3
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13
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253

abundance is found at 25 m depth, below which a gradual decrease inabundance occurs to 50 m depth; the deepest individuals occur at
95 m (Yordanova and Hohenegger, 2002). Calcarina mayori also lives
in a wide range of water depths (10–70 m), although its optimal
depth is around 30 m (Hohenegger, 2004).
The above ﬁndings indicate that the difference between the two
species in terms of their temporal and spatial distributions within the
cave cannot be explained by light intensity alone. One possible
interpretation is microhabitat differences between the two species.
Although the two species prefer hard (macroalgae and reef rubble)

84

48

180

substrates (Hohenegger, 2004; Renema, 2006), Heterostegina depressa
is also found on sand (Hohenegger et al., 1999). Heterostegina depressa
is characterized by weaker attachment than C. mayori. Thus, H.
depressa avoids settling in exposed smooth surfaces to resist
entrainment by hydrodynamics (Fujita, 2004), whereas C. mayori
can attach to the smooth surface of hard substrates (Hohenegger et al.,1999). H. depressa also shows a clear preference for horizontal or
oblique surfaces, and tends to avoid vertical surfaces (Renema, 2006).
These observations suggest that H. depressa can live on reef rubble andcalcareous sands on gentle slopes near the cave entrance, while C.

A. Omori et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 292 (2010) 443–452

451

Fig. 7. Spatial distributions of algal symbiont-bearing large benthic foraminifer species in Daidokutsu Cave. The locations of sites a–f, Core 4, and fore-reef samples are shown in
Figs. 1 and 2.

mayori can live attached to roofs and vertical walls inside the cave.
Another possible interpretation is space competition proposed by
Hohenegger (2004), which showed that the density of H. depressa was
suppressed by the co-occurrence of C. mayori.
Amphistegina bicirculata occurs continuously within the sedimentfrom both the central part of Daidokutsu Cave (Core 06) and theinnermost part (Core 19) (Figs. 4 and 5). The species lives on hard, gravel
and coarse sand substrates in water depths of 30–130 m (Yordanova
and Hohenegger, 2002; Hohenegger, 2004), particularly favoring thelower part of the euphotic zone (optimal depth of 80 m; Yordanova andHohenegger, 2002). Tests of A. bicirculata are found in the innermost
part of the cave (Fig. 7), and ﬁve living individuals were found within thesurface sediment at site 1 (Table 1). These ﬁndings suggest that the
specimens of this species are indigenous, living on calcareous sand,skeletal remains of macroinvertebrates, roofs and walls inside the cave,and that the innermost part of the present-day cave is a favorable
environment for survival of the species. The abundance of A. bicirculata
in sediment from the inner area of the cave (Core 19) shows a gradualincrease until 5000 yr BP (Fig. 5). Considering a gradual increase inabundance of A. bicirculata and C. mayori, as well as decreases inabundance of LBF species commonly found near the cave entrance
discussed above, the interior of the cave is considered to have becomedarker during the period leading up to 5130 yr BP. The darkness
corresponds to the light intensity at 50–70 m water depth in the open
sea, which is based on the overlap range between the depth
distributions of A. bicirculata and C. mayori.
Because the gradual darkening of the cave was synchronous with
reduced inﬂow of material from the open sea (debris from the red soil
layer), it is likely that the inﬁlling of cavities and narrowing of the caveentrance occurred up to 5130 yr BP, which were probably caused by
the development of reef-front and fore-reef zones and the transport ofcobbles and boulders to the entrance. The decline in light intensity led
to a decrease in photosynthetic production within the cave. In

addition, the reduction in water exchange between the interior andexterior of the cave appears to have resulted in a reduction in the
supply of various materials into the cave (e.g., dissolved inorganic andorganic matter, and bacterioplankton) that are essential for bothheterotrophs and autotrophs. Therefore, the ﬁndings of this study
support Kitamura et al.'s (2007a) hypothesis that the inﬁlling ofcavities and narrowing of the cave entrance caused a millennia-scaledecline in food supply within the cave, thereby affecting the species
compositions of cavernicolous bivalves.
Acknowledgments
We thank Dr. Takao Ubukata, Shigemitsu Kinjo, Koushin Yasumura
and Syu-ichi Ohashi for their kind advice and for collecting samples
for analysis. We thank A. Stallard for improving the English in the
manuscript. We also thank Dr. J. Hohenegger and one anonymous
reviewer for comments on the manuscript. This study was funded by
Grants-in-Aid 16340159 and 19540492 awarded by the Japan Society
for Promotion of Science, The Japan Science Society, a Sasakawa
Scientiﬁc Research Grant, and a Grants-in-Aid from the Fukada
Geological Institute.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.palaeo.2010.04.004.
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