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DIVERSITY AND PALEOECOLOGY OF MIOCENE CORAL-ASSOCIATED MOLLUSKS FROM EAST KALIMANTAN (INDONESIA) Source: PALAIOS, 30(1):116-127. Published By: Society for Sedimentary Geology URL: http://www.bioone.org/doi/full/10.2110/palo.2013.124

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PALAIOS, 2015, v. 30, 116–127 Research Article DOI: http://dx.doi.org/10.2110/palo.2013.124

DIVERSITY AND PALEOECOLOGY OF MIOCENE CORAL-ASSOCIATED MOLLUSKS FROM EAST KALIMANTAN (INDONESIA) ARIES KUSWORO,1 SONJA REICH,2 FRANK P. WESSELINGH,2 NADIEZHDA SANTODOMINGO,3 KENNETH G. JOHNSON,3 JONATHAN A. TODD,3 AND WILLEM RENEMA2 1

Pusat Survei Geologi, Jl. Diponegoro 57, Bandung 40122, Indonesia Naturalis Biodiversity Center, Department of Geology, P.O. Box 9517, 2300 RA Leiden, The Netherlands 3 Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW& BD, UK e-mail: [email protected]

2

ABSTRACT: This study is a preliminary assessment of an extremely diverse Tortonian (late Miocene) mollusk assemblage from a coral carpet environment preserved at Bontang (East Kalimantan, Indonesia). Even though coral-associated aragonitic faunas are rarely well preserved, the composition of the assemblage described here can be used to address the following questions: (1) How do the mollusk assemblages in coral habitats differ from other habitats, and (2) What is the effect of sampling on estimates of taxon richness? The mollusk assemblage is dominated by predatory snails and includes typical modern coralassociated taxa such as the gastropod Coralliophila and the bivalve Tridacna. Our investigation implies that adequate documentation of Cenozoic mollusk diversity in the Indo-Pacific is even more challenging than previously expected as very large samples are required to capture species richness. Further assessments of fossil faunas from coral-dominated habitats will be required to provide insight to development of Indo-Pacific biodiversity through time.

INTRODUCTION

The Indo-West Pacific (IWP), extending from the Red Sea and East Africa to the Central Pacific, is the largest of four major oceanic biogeographic regions, and the one holding the highest taxon diversity (Ekman 1934; Briggs 1974; Paulay 1997). Within the IWP, the center of maximum marine biodiversity (species richness) is located in the IndoMalayan region where local species richness peaks in and around coral habitats (Hoeksema 2007; Renema et al. 2008). A large variety of organisms, including corals, fish, mollusks, crustaceans, and echinoderms contribute to the high diversity in the region (Bellwood et al. 2005; Hoeksema 2007; Renema et al. 2008). Documentation of the fossil record is required in order to understand the ecological and environmental context of the origin of the biodiversity hotspot, as well as its development through time (Renema et al. 2008). Although the sampling of ancient coral reef–associated habitats is necessary to document levels of biodiversity, this is frequently difficult: coral facies often suffer strong diagenesis, compromising the preservation of associated organisms, especially those with aragonitic hard-parts, such as mollusks (Wright et al. 2003). This results in highly biased mollusk assemblages from reefal environments that are largely made up of taxa with more diagenetically resistant and largely calcitic shells, such as oysters and pectinids (Wright et al. 2003, and references therein; Santodomingo et al. 2015). In this study an unusually well preserved association of ramose corals and mollusks from upper Miocene deposits in Bontang (East Kalimantan, Indonesia) is presented. The material provides the opportunity to investigate a rare Neogene coral-associated mollusk assemblage from the IWP biodiversity hotspot. The aim of this study is to reconstruct the paleoenvironment and to characterize the mollusk assemblage in terms of diversity and ecology. Specific questions that we address include: (1) How do the mollusk assemblages in coral habitats differ from other habitats, Published Online: February 2015 Copyright E 2015, SEPM (Society for Sedimentary Geology)

and (2) What is the effect of sampling on taxon richness estimates? To achieve these goals we reconstruct the paleoenvironment of the locality, document the mollusk assemblage in terms of taxon richness and feeding guild composition, and compare our results to published faunas from elsewhere in the IWP. GEOLOGICAL SETTING AND STUDY LOCALITY

The Miocene outcrops of Bontang are located on the eastern side of the Kutai Basin, the southeasternmost extension of the Sunda platform on the east coast of Kalimantan, Indonesia. The Kutai Basin is confined by the Sangkulirang fault zone in the north, the Adang fault zone in the south, the Kalimantan High in the west, and to the east the Makassar Strait. The formation of the Kutai Basin initiated during the Eocene (Moss and Chambers 1999). Subsequently the basin developed in various phases during the Cenozoic, including major changes of the basin architecture and depositional systems. During the late Neogene and Quaternary the basin development was regressive, a result of sediment fill, inversion, and uplift (Allen and Chambers 1998). In Miocene times the study area was located in a coastal zone that received considerable input of terrigenous clastic sediments (Cibaj 2009; Marshall et al. 2015). In spite of relatively turbid water conditions, rich coral communities could develop in the region (Wilson 2005; Novak et al. 2015; Santodomingo et al. 2015). The sampling locality TF 102 (0.16821u N, 117.44350u E) is an abandoned quarry on the north side of the northern entrance road to Bontang (Fig. 1). The locality represents the upper part of a marine interval of about 150 cm of fossiliferous, coarsening-upward, silty clay to fine sandy silt (Fig. 1). Below this interval gray-blue clay with dispersed fossiliferous lenses occurs. Above the marine interval lies a nonfossiliferous undulating clay bed of approximately 160 cm thickness

0883-1351/15/030-116/$03.00

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FIG. 1.—Overview over locality TF 102, Bontang, East Kalimantan. A) Location in the Bontang area. B) Situation sketch of coral patches on the floor of abandoned quarry TF 102. C) Lithological column of the TF 102 quarry section: a 5 clay, b 5 silt, c 5 sand, d 5 organic matter, e 5 shells, f 5 corals. The asterisk denotes the sampled interval. Height in meters.

followed by approximately three meters of barren fine sandstones. Those sediments represent the basal part of an overlying fluvial unit. Biostratigraphic data (large benthic foraminifera and calcareous nannoplankton) suggest that the TF 102 locality and other fossiliferous localities nearby are assigned a Tortonian age (Renema et al. 2015). Strontium isotope data from scleractinian corals and giant clams (Tridacninae) from six localities in the Bontang area (including TF 102) show ages ranging from 8.24 Ma to 9.75 Ma (61 Ma) with an average of 9.4 6 0.2 Ma, matching a Tortonian biostratigraphic age (Renema et al. 2015). MATERIAL AND METHODS

Fossil mollusk and coral assemblages were collected from discrete patches of fragmented ramose corals, weathering out on the approximately horizontal surface of a bedding plane of marine silts and clays (Figs. 1, 2). Although these patches had been rainwashed, leading to some concentration of the fauna, specimens showed no signs of lateral transport. In addition, many of the thinner-shelled mollusks were whole, suggesting patches had been exposed on the quarry floor for only a short period of time. This is confirmed by the lack of any surficial features on

FIG. 2.—Images of the surface of a coral-mollusk patch on the floor of the TF 102 quarry. A) Coral fragments and mollusks; a larger muricid gastropod is visible in the center. B) Melongena in the center; the smaller gastropod shell in front is a Coralliophila. C) A comparatively large strombid shell on the left.

larger mollusks that might indicate partial dissolution of aragonite. Therefore we could largely discount compositional distortion through atmospheric weathering of the recovered assemblage. The size and shape of each coral patch was measured along a line transect of 10 m length. A

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A. KUSWORO ET AL. TABLE 1.— Mollusk data and feeding ecology. For abbreviations of feeding guilds see Figure 6.

Taxon

FG

SR50

SR51

SR52

SR53

SR54

Total

Diodora sp. 1 Stomatolina sp. 2 Gibbula leupoldi Beets, 1941 ?Gibbula sp. 1 Trochidae indet. sp. 1 Angaria aff. spaerula (Kiener 1873) sensu Beets, 1942 Bothropoma sp. 1 Smaragdia semari Beets, 1941 Cerithium sp. 3 Cerithium sp. 7 Colina sp. 1 Rhinoclavis sp. 1 s.l. Diala semistriata s.l. (Philippi 1849) Modulus praeangerensis Martin, 1905 ?Potamididae indet. sp. 1 Finella sp. 3 Ampullina s.l. sp. 2 Ampullospira sp. 1 Ampullospira sp. 2 Plesiotrochus sp. 6 ?Capulus sp. 2 Eatoniella s.l. sp. 3 Natica helvacea Lamarck, 1822 sensu Beets, 1941 Rissoina (Phosinella) sp. 2 Rissoina indet. Rissolina sp. 2 Cyclostremiscus novemcarinatus (Melvill 1906) sensu Beets, 1986 Canarium unifasciatum s.l. (Martin 1884) Strombus s.l. sp. 2 Strombus s.l. sp. 3 Strombus s.l. sp. 4 Varicospira sp. 1 Terebellum sp. Cymatium (Reticutriton) sp. 1 Cymatium (Turritriton) cf. tenuiliratum (Lischke 1873) Ranellidae indet. sp. 2 Eratoena sp. 1 Epitonium sp. 3 Triphora s.l. sp. 3/Triphora indet. [Beets] Seila sp. 1 ?Buccinidae indet. sp. 1 Euplica sp. 1 Mitrella s.l. cf. gembacana (Martin 1921) Mitrella s.l. njalindungensis sensu (Beets 1941) non (Martin 1921) Zafra sp. 1 Mitrella s.l. sp. 1 Mitrella s.l. sp. 2 Mitrella s.l. sp. 3 Mitrella s.l. sp. 4 ?Pyreneola sp. 1 Peristernia beberiana sensu Beets, 1941 non Martin, 1921 Chicoreus sp. 1 Chicoreus sp. 2 Coralliophila aff. clathrata (A. Adams 1854) Coralliophila sp. 2 Coralliophila sp. 3 ?Muricidae indet. sp. 1 Melongena sp. 1 Nassarius sp. 2 Nassarius sp. 3 Nassarius sp. 4 Nassarius sp. 5 Vexillum sp. 9 Vexillum sp. 11 Vexillum sp. 12 Vexillum sp. 14 Vexillum sp. 15 Vexillum sp. 16

H H H H H H H H H H H H H H H H H H H H SU H CP H H H H H H H H H H CP CP CP CB CB CB CB CP CP CP CP CP CP CP CP CP CP CP CP CP CB CB CB CP CP CP CP CP CP CP CP CP CP CP CP

2 0 5 0 0 0 1 6 3 24 7 0 2 0 0 1 1 2 3 14 0 1 2 5 0 3 0 14 0 0 2 0 1 0 0 1 0 0 3 1 1 1 4 2 14 2 0 0 0 1 2 0 1 3 2 5 0 0 19 7 0 7 4 5 4 4 1 0

2 0 2 1 1 0 0 1 2 21 5 0 4 0 2 0 0 2 0 13 0 0 4 2 0 1 0 3 0 0 0 0 1 0 1 0 0 0 2 0 1 0 1 1 10 0 0 0 0 0 0 2 0 3 0 1 0 0 9 5 0 4 1 6 5 0 0 1

1 0 2 0 0 1 0 2 0 4 2 0 1 0 0 0 0 0 0 1 0 0 0 0 0 1 0 1 0 0 0 0 0 1 0 0 0 0 2 0 0 0 1 1 2 0 0 0 0 0 1 0 0 2 0 0 0 1 7 2 0 1 1 1 0 1 0 0

2 1 11 2 0 0 0 5 13 48 0 0 10 4 0 0 0 1 2 18 0 0 4 8 0 4 0 7 1 0 0 1 0 0 0 0 0 0 5 1 1 4 5 4 23 2 1 0 0 0 7 4 0 7 0 1 2 0 13 16 2 19 8 5 0 5 0 0

2 0 4 0 0 0 0 1 7 10 0 1 9 1 0 0 0 0 1 8 1 0 8 2 1 0 1 8 2 1 0 0 1 0 0 0 1 1 3 0 0 0 6 2 10 0 0 1 1 0 1 0 0 1 0 3 0 0 7 1 0 4 2 4 0 1 0 0

9 1 24 3 1 1 1 15 25 107 14 1 26 5 2 1 1 5 6 54 1 1 18 17 1 9 1 33 3 1 2 1 3 1 1 1 1 1 15 2 3 5 17 10 59 4 1 1 1 1 11 6 1 16 2 10 2 1 55 31 2 35 16 21 9 11 1 1

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TABLE 1.— Continued. Taxon

FG

SR50

SR51

SR52

SR53

SR54

Total

Vexillum sp. 17 Cystiscus sp. 3 Granulina menkrawitensis (Beets 1986) Granulina sp. 2 Cryptospira sp. 1 Cryptospira sp. 2 Dentimargo sp. 1 Marginellidae indet. Mitra sp. 1 Mitra sp. 2 Mitra sp. 4 Mitra sp. 5 Olivella sp. 2 Dendroconus odengensis s.l. (Martin 1895) Conidae indet. sp. 3 Conidae indet. sp. 4 Conidae indet. sp. 5 Conidae indet. sp. 6 Hemilienardia sp. 1 Lienardia sp. 2 Clathurellidae indet. sp. 1 Clathurellidae indet. sp. 2 Eucithara sp. 5 Eucithara sp. 6 Eucithara sp. 7 Raphitomidae indet. sp. 3 Raphitomidae indet. sp. 4 Raphitomidae indet. sp. 5 Tomopleura sp. 1 Iredalea sp. 1 Tylotiella sp. 2 Drilliidae indet. sp. 2 Inquisitor sp. 3 Pseudomelatomidae indet. sp. 4 Pseudomelatomidae indet. sp. 5 Pseudomelatomidae indet. sp. 6 Strictispira sp. 2 Strictispira sp. 3 Lophiotoma sp. 1 Terebra s.l. sp. 2 Adelphotectonica karikalensis (Cossmann 1910) sensu (Beets 1941) Linopyrga sp. 1 Odostomiinae indet. sp. 1 Pyramidella sp. 2 ?Tibersyrnola sp. 1 Pyramidelloidea indet. sp. 1 Pyramidelloidea indet. sp. 2 Pyramidelloidea indet. sp. 3 Talahabia cf. dentifera Martin, 1921 Cylichna s.l. sp. 2 Cylichna s.l. sp. 3 Pupa sp. 2 Gastropoda indet. spp. Nucula sp. 1 Brachidontes sp. 1 Modiolus sp. 1 Acar sp. 1 Anadara sp. 3 ?Barbatia sp. 1 Arcopsis sculptilis sensu Beets, 1941 Pteria s.l. sp. 1 ?Malleus s.l. sp. 1 Dendostrea sp. Lopha sp. 1 Ostreidae indet. Mimachlamys aff. menkrawitensis (Beets 1941) Chlamys s.l. sp. 1 Spondylus sp. 2

CP CB CB CB CB CB CB CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CP CB CB CB CB CB CB CB CB CB CP CP CP CP SU SU SU SU SU SU SU SU SU SU SU SU SU SU SU

0 2 0 0 3 1 4 0 0 2 0 0 3 0 2 1 3 1 1 1 1 1 2 4 0 1 0 0 1 2 0 0 0 0 0 0 2 0 23 0 0 0 0 0 0 1 0 0 1 0 1 0 17 0 0 0 2 13 0 18 1 0 11 0 1 3 0 0

0 0 0 0 0 0 6 2 0 0 1 0 0 1 1 0 0 0 0 0 1 0 1 1 0 0 2 0 0 8 0 0 0 1 0 0 0 0 15 1 1 1 0 0 1 0 0 0 1 0 0 1 20 0 0 0 0 6 0 7 0 1 14 0 3 2 1 0

0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 2 0 0 0 1 0 5 0 0 0 0 0 0 2 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 4 0 0 0 0 1 0 2 0 0 4 0 1 1 1 0

1 9 0 1 2 0 7 0 1 0 0 1 3 1 2 3 0 0 1 0 2 0 5 4 1 1 0 0 0 12 3 0 1 0 0 0 2 1 30 0 0 1 1 0 1 0 1 1 0 0 0 0 59 0 1 1 1 13 1 19 2 1 26 0 5 6 2 0

0 0 1 0 0 0 5 0 1 0 0 0 2 0 0 0 0 0 1 3 0 0 3 2 0 0 0 1 0 11 1 2 0 0 1 1 2 0 9 0 1 0 0 1 0 0 0 0 2 2 0 0 13 1 1 0 2 8 1 7 1 0 11 2 5 1 1 1

1 11 1 1 5 1 23 3 2 2 1 1 8 2 5 4 3 1 3 4 4 1 12 13 1 2 2 2 1 38 4 2 1 1 1 1 8 1 78 1 2 2 1 1 2 1 1 1 4 2 1 1 113 1 2 1 5 41 2 53 4 2 66 2 15 13 5 1

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A. KUSWORO ET AL. TABLE 1.— Continued.

Taxon

FG

Plicatula sp. 1 Cardiolucina sp. 2 Cardita s.l. sp. 3 Trachycardium denticostulatum (Beets 1941) Vasticardium sp. 1 Cardiidae indet. sp. 6 Cardiidae indet. sp. 7 Tridacna (Chametrachea) mbalavuana Ladd, 1934 Chama sp. 1 ? Tellina s.l. sp. 3 Tellina s.l. sp. 4 Tellina s.l. sp. 5 Tellina s.l. sp. 6 Circe ickeae sensu (Beets 1941) non Martin, 1922 Dosinia sp. 1 Gafrarium sp. 1 ?Timoclea sp. 1 ?Timoclea sp. 2 Veneridae indet. sp. 3 Veneridae indet. sp. 4 Veneridae indet. sp. 5 Corbula solidula Hinds, 1843 sensu Beets 1941 Corbula sp. 1 Corbula sp. 2 Pholadidae indet. sp. 1 Polyplacophora indet. sp. 1

SU CD SU SU SU SU SU SU SU D D D D SU SU SU SU SU SU SU SU SU SU SU B H

total specimens total species

total of five coral patches, each with an area of about 1–3 m2, were studied (Fig. 1). The first set of samples was obtained by handpicking every mollusk seen at the surface of each coral patch. One additional handpicked surface collection includes larger, well-preserved coral colonies, selected to complement the taxonomic inventory. Subsequently, two bulk sediment samples were collected from each patch, resulting in a total of 10 bulk samples with weights ranging from 3 to 6 kg. One of each of the paired samples (numbered for each site: SR50 to SR54) was used to study the taxonomic and ecological composition of the mollusk assemblage. The second sample of each pair (numbered for each site: NS50 to NS54) was used to study the composition of the coral assemblage. Bulk samples used for the study of mollusks were treated following the procedures outlined in Reich et al. (2014), assessing all mollusk remains retained on a sieve with a mesh of 1 mm. Counting of specimens was likewise done as described in Reich et al. (2014). Taxonomic identifications follow publications on fossil faunas of Indonesia (Beets 1941, 1986; Leloux and Wesselingh 2009; Reich et al. 2014) as well as descriptions of modern Indo-Pacific faunas (e.g., Okutani 2000; Poppe 2008a, 2008b, 2008c, 2010). Specimens that could not be identified due to their poor preservation are labeled as Gastropoda or Bivalvia indet. spp. and are excluded from statistical analyses. The mollusk material is housed in the collection of Naturalis Biodiversity Center, Leiden, The Netherlands (indicated by RGM numbers). Bulk samples used for the study of corals were soaked in water, washed, and sieved. The size fraction retained on a sieve mesh of 3.5 mm was studied. Identifications of corals are based on macro- and micromorphological features of colonies and corallites, following taxonomic accounts of Indonesian fossil faunas (Gerth 1921, 1923; Umbgrove 1929; mostly illustrated by Leloux and Renema 2007). Taxon names were assigned according to the recent revision of Indo-Pacific fossil

SR50

SR51

SR52

SR53

SR54

Total

0 2 2 0 0 0 2 1 3 0 0 0 0 2 0 3 0 0 1 0 0 4 1 0 0 0

0 1 1 1 0 0 0 0 3 0 0 0 0 2 0 1 1 0 0 0 0 2 0 0 0 0

1 0 0 0 0 1 3 0 2 1 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0

0 1 2 1 1 1 4 0 15 0 0 1 1 4 2 3 1 1 0 2 1 4 0 0 0 0

0 2 1 0 0 0 2 0 7 0 1 1 0 4 0 0 0 0 0 0 0 0 0 1 1 1

1 6 6 2 1 2 11 1 30 1 1 2 1 12 2 8 2 1 1 2 1 11 1 1 1 1

344 84

232 67

78 46

558 97

246 80

1458 163

corals by Johnson et al. (2015). Specimens identified as Acropora were classified into morphological species groups sensu Wallace (1999). The coral material is deposited in the collections of the Natural History Museum, London, UK (indicated by NHMUK numbers). According to the state of preservation and the available taxonomic frameworks, both mollusks and corals were identified to the lowest possible rank (species). Otherwise, taxa were left in open nomenclature indicating their genus or family. Because part of the assemblages could not be identified below family level, the term taxon is used in this study rather than species. In addition to the taxonomic classification, feeding guilds of mollusk taxa were defined as outlined in Reich et al. (2014). Coral abundances were estimated based on number of colony fragments as well as on weight of material (dry weight in grams) of each taxon per coral patch. The sampling adequacy was explored using sample rarefaction, also providing an estimate of mollusk diversity. Analysis was performed using PAST (Paleontological Statistics; Hammer et al. 2001). We tested for statistical differences between the samples using Raup-Crick dissimilarities. Raup-Crick dissimilarities were calculated to assess how taxonomic composition varied among the assemblages, using the vegan package in the R statistical programming environment (Oksanen et al. 2013; R Core Team 2013). The method is specifically designed for cases where sampling is incomplete and uneven among sites, because Raup-Crick dissimilarities are based on the probability that the compared sampling units have nonidentical compositions (Raup and Crick 1979). Two versions of RaupCrick dissimilarities were applied. The first is based on analytic results of a hypergeometric distribution to find probabilities with the underlying assumption that all species occurrences are equally probable. The second is based on permutation results that allow sampling probabilities to be proportional to species frequencies. Raup-Crick dissimilarity for almost identical assemblages is close to zero. Raup-Crick dissimilarity for two assemblages with only a few shared species is close to 1.

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MIOCENE INDONESIAN CORAL-ASSOCIATED MOLLUSKS RESULTS

Taxonomic Composition of the Mollusk Assemblage A total number of 178 identified mollusk taxa were obtained from the samples (Table 1). The five surface collections contained on average 31 taxa (ranging from 17 to 54). The five bulk sediment samples contained on average 70 taxa (ranging from 45 to 96). The overall most abundant taxa are illustrated in Figure 3. Twenty-four species were present only in surface-collected samples, whereas 102 species only occurred in bulk samples. Gastropods represent the most abundant and most species-rich mollusk group in all samples. They make up more than 70% in terms of specimens and species numbers in bulk samples. Bivalves make up around a quarter of the assemblage. A single polyplacophoran plate was found. Taxon abundance is highly skewed, with few abundant and many rare taxa. Sample Size and Dissimilarity The rarefaction curves show undersaturation for all samples, especially for the hand-picked surface collections (Fig. 4). Because rarefaction curves unambiguously showed that the surface-picked collections were too small to provide enough data to accurately characterize assemblage composition and taxon richness (Fig. 4), we excluded them from further analyses. Raup-Crick sample dissimilarity of all five bulk samples using equal probability ranges from 0 to 0.18 (mean 5 0.02, Table 2A). Using abundance-based dissimilarities, sample SR50 differs from almost all other samples apart from sample SR52 (Table 2B). RaupCrick dissimilarity between SR50 and SR54 is highest. A moderate dissimilarity is seen between SR50 and samples SR51 and 53. The only other samples that display a moderate dissimilarity are samples SR51 and 54. The most abundant mollusk taxon in bulk samples is a medium-sized (,10 mm) cerithiid (Fig. 3G). The second most abundant taxon is a comparatively large (,25 mm) turrid (Lophiotoma sp. 1, Fig. 3R). The next most abundant taxa in bulk samples are represented by the genera Dendostrea, Zafra, Nassarius, Plesiotrochus, Arcopsis, Anadara, and Iredalea (Fig. 3). The five most abundant taxa in the surface samples are Lophiotoma sp. 1, Corallliophila aff. clathrata, Natica helvacea, Cryptospira sp. 1, and Euplica sp. 1. These represent the 2nd, 22nd, 19th, 47th, and 48th most important species in the bulk samples. Ecological Composition of the Mollusk Assemblage Feeding ecology was reconstructed for the assemblage obtained from adding all bulk-sample patches together (Table 1). The assemblage is dominated by predatory and scavenging carnivorous gastropods, both in terms of species numbers (55%) and in abundance (48%). The most numerous carnivore, Lophiotoma sp. 1 (Fig. 3G), belongs to the superfamily Conoidea, which is represented by a total of 25 taxa (193 specimens) in the sampled assemblage as a whole. The likewise abundant Iredalea (Fig. 3G) is a conoidean as well. Both genera were formerly lumped together in the Turridae, the members of which commonly prey on polychaetes (Beesley et al. 1998; Bouchet et al. 2011). Nassariidae are also common, represented by four species (123 specimens; Fig. 3N–P), two of which are among the ten most abundant taxa. Members of the family largely feed on carrion, although they may shift facultatively to plant matter (Brown 1969). Suspension feeders and herbivores (including detritivores) typically make up about a quarter of the assemblage. The latter group is slightly more prominent (28%) in the abundance dataset. Suspension feeders are represented by bivalves, apart from a single capulid gastropod. Within the suspension-feeding bivalves, shallow infaunal as well as epifaunal taxa are present. Whereas infaunal and epifaunal bivalves are represented by the same number of taxa, epifaunal

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bivalves are much more abundant and make up almost 80% of the bivalve assemblage in terms of specimens. This is due to the presence of a few very abundant taxa, such as Dendostrea and Arcopsis (Fig. 3B, C). The most abundant herbivorous/detritivorous gastropods are Cerithium, Plesiotrochus, and Canarium unifasciatum (Fig. 3G–I, K). The obligate seagrass-feeding gastropod Smaragdia (Rueda et al. 2009; Unabia 2011) is present in low numbers. Browsing carnivores are the least abundant gastropod feeding guild present. The guild is more prominent in species richness than in abundance. The most common taxon is the marginellid Dentimargo, followed by the coral feeder Coralliophila (Fig. 3L), and Triphora, an ectoparasite on sponges. The most speciesrich, though not very abundant, group included in the latter guild are the ectoparasitic pyramidelloids. Infaunal, deposit-feeding bivalves include tellinids and chemosymbiotic deposit feeders, the latter represented by a species of Cardiolucina (Fig. 3D). Both families contribute little to the abundance and species richness of mollusks from the sampled units (, 1% to 2%). Taxonomic Composition of the Coral Assemblage Nineteen coral taxa were identified from the bulk sediment samples. Material from handpicked surface collections was better preserved and included larger colonies, but did not yield any additional taxa (Table 3). Taxon abundances measured as weight of colonies indicate that corals are mainly represented by ramose forms (67.5%) with subordinate columnar forms (21.5%). The most abundant ramose corals are taxa in the genus Dictyaraea (50.2%; Fig. 5A–C). Of these, three taxa could be identified as Dictyaraea sp. 1 (29.6%), Dictyaraea sp. 2 (19.2%), and Dictyaraea micrantha var. spinosa (1.4%). Other abundant ramose corals are Alveopora sp. (13.2%), Seriatopora irregularis (2.6%), and Acropora sp. aspera group (1.5%). Columnar forms include Platygyra sp. (9.6%) and Goniopora sp. (5.9%). Other coral forms make up less than 10% of the total assemblage. They include among others a free-living mushroom coral (Fungia sp.), fragments of small massive Oulophyllia sp., and the flabello-meandroid Trachyphyllia sp. No significant difference was seen when abundances were estimated as number of colony fragments. DISCUSSION

Paleoenvironment Corals are abundant at the sampling locality, but they form small thickets, evidently following the seafloor morphology instead of forming build-up structures. We therefore refer to the paleoenvironment as a coral carpet sensu Riegl and Piller (2000). The dominance of ramose forms in the coral assemblage is interpreted as a response to high sedimentation rates and high turbidity in the water column, because ramose colonies are more likely to overcome potential burial and suffocation caused by constant or episodic sediment discharge (Sanders and Baron-Szabo 2005; Reuter et al. 2012). Among the ramose corals present, Dictyaraea species are the most abundant in our samples. Dictyaraea is an extinct genus of the family Poritidae, with its oldest fossil occurrence in the Oligocene of France (Chevalier 1956). The genus is commonly reported from Miocene fossil coral faunas of Indonesia (Gerth 1923; Umbgrove 1929; Johnson et al. 2015) and became extinct in the Pleistocene (Johnson et al. 2015). Modern representatives of the family Poritidae in reefal habitats include the genera Porites and Goniopora. Both genera include species that are common in relatively calm waters and that tolerate comparatively high input of sediments into their habitat (Stafford-Smith and Ormond 1992). Assuming Dictyaraea shares similar ecologies with its modern counterparts, it is inferred that these sedimenttolerant coral assemblages occupied calm, shallow waters influenced by high siliclastic input habitats in the Miocene of East Kalimantan.

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FIG. 3.—Common mollusk taxa in the TF 102 fauna, and some characteristic ecological indicator species. All scale bars 5 1 mm. A) Anadara sp. 3, RGM 793.987, W 9.9 mm. B) Arcopsis ? sculptilis, RGM 793.986, W 5.0 mm. C) Dendostrea sp. 1, RGM 793.965, L 18 mm. D) Cardiolucina sp. 2, RGM 793.967, W 4.4 mm. E) Chama sp. 1, RGM 793.992, H 5.5 mm. F) Gibbula leopoldi, RGM 793.994, H 6.6 mm. G) Cerithium sp. 7, RGM 793.966, H 9.5 mm. H) Plesiotrochus sp. 6, RGM 793.985, H 7.6 mm. I) Cerithium sp. 3, RGM 793.993, H 9.6 mm. J) Diala semistriata s.l., RGM 793.995, H 2.9 mm. K) Canarium unifasciatum s.l., RGM 793.990, H 15.5 mm. L) Coralliophila aff. clathrata, RGM 793.969, H 16.2 mm. M) Zafra sp. 1, RGM 793.983, H 2.9 mm. N) Nassarius sp. 2, RGM 793.984, H. 5.7 mm. O) Nassarius sp. 5, RGM 793.988, H. 4.7 mm. P) Nassarius sp. 3, RGM 793.991, H. 7.1 mm. Q) Iredalea sp. 1, RGM 793.989, H 4.7 mm. R) Lophiotoma sp. 1, RGM 793.968, L 25 mm.

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FIG. 4.—Rarefaction curves. A) Mollusk richness of the TF 102 samples including surface-collected samples (SR45–SR49) and bulk samples (SR50–SR54). B) richness of the entire TF 102 fauna compared to an early Miocene seagrass fauna from Banyunganti (Java, Indonesia; data from Reich et al. 2014).

Fossil mollusks were predominantly observed within the coral patches and not in the sediments in between. This suggests that the occurrence of mollusks is associated with the presence of corals in the studied environment. Therefore, we assume that Dictyaraea corals offered a microhabitat that supported the rich mollusk community presented in this study. The assumed high rates of clay-grade sedimentation probably provided a preservation window for the aragonitic mollusks. Close association of components of the mollusk assemblage to the once-living coral assemblage is also indicated by the presence of the obligate coral grazer Coralliophila (Beesley et al. 1998). Furthermore, fragments of the reef-associated bivalve Tridacna were recovered from the quarry floor and in some of the samples. The high abundance of the small epifaunal ostreid genus Dendostrea may indicate the presence of gorgonians (sea whips, sea fans) in the environment, the preferred substrate of modern Dendostrea frons in tropical America (Forbes 1971). Although the assemblage is assumed to be largely taphonomically unbiased, we cannot exclude the possibility that the numerical dominance of that taxon is due to its higher preservation potential because of its calcitic shell. Possibly thinner-shelled bivalve taxa were more affected by weathering and fragmentation and were therefore not included in the sampled assemblages. TABLE 2.— Raup-Crick sample dissimilarity. A) Equal probability. B) Proportional to species abundance. A.

Patch1

Patch2

Patch3

Patch4

Patch2 Patch3 Patch4 Patch5

0.0103 0.0001 0.0109 0.1807

0.0000 0.0004 0.0391

0.0000 0.0000

0.0003

B.

SR50

SR51

SR52

SR53

SR51 SR52 SR53 SR54

0.497 0.049 0.545 0.936

0.001 0.121 0.704

0.008 0.013

0.136

In addition, some shells of the obligate seagrass-feeding gastropod Smaragdia (Reich et al. 2015) were found. Specimen numbers are very low, but they are equally well preserved as the other taxa (no surface wear, similar coloration). Thus we assume that they were part of the original life assemblage (e.g., Kidwell and Bosence 1991; Kidwell and Flessa 1996; Kidwell 2008). Therefore, we conclude that interspersed seagrasses or seagrass patches were present in this habitat, as is frequently seen in modern coral carpets. Variation among Samples The relatively low numbers of specimens in the hand-picked samples and the observed differences in the composition of the hand-picked versus bulk samples confirm that the hand-picked samples cannot be used to meaningfully address taxon richness in mollusk assemblages. Overall, the very low Raup-Crick dissimilarities among samples indicate little variation in their taxonomic composition. Therefore, the samples from different coral patches represent a single coral-associated mollusk community, albeit sampled over a small horizontal distance. This justifies the combined analysis of all five merged bulk samples as a single assemblage. The high abundance-based dissimilarity between sample SR54 and samples SR50 and SR51 is probably due to comparatively low abundances of overall very common species, such as Cerithium sp. 7 and Lophiotoma sp. 1 in sample SR54 (e.g., 59 specimens of Ceritium sp. 7 in SR51 vs. 13 specimens in SR54). Combining the bulk samples is needed to develop a realistic estimate of overall richness, as the sample size of each of the bulk samples individually (100–500 specimens) is insufficient to produce a realistic sampling distribution when total richness is at least 178 taxa. Comparison with Other Faunas Few faunas have been analyzed using a comparable approach and are available for comparison. Even though the total number of observed taxa in the early Miocene Banyunganti fauna (Reich et al. 2014) is higher, the sampling curve of the TF 102 fauna is steeper. The rarefaction curve shows that the overall species richness of the seagrass assemblage is lower than that of the coral carpet assemblage (Fig. 4).

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TABLE 3.—Coral taxa abundances and growth forms. Data is presented as the dry weight of each taxon in grams and the number of fragments per sample. Ra 5 ramose, Co 5 columnar, Ma 5 small massive, Pl 5 platy, Fm 5 flabello-meandroid, Fr 5 free-living. Weight in grams Taxon

Form

NS50

NS51

NS52

NS53

NS54

Hand picked

Total

%

Dictyaraea sp.1 Dictyaraea sp.2 Dictyaraea micrantha Porites sp. Goniopora sp. Seriatopora irregularis Seriatopora hystrix Stylophora sp. Acropora sp. aspera group Alveopora sp. Montipora sp. Fungiidae sp. Leptastrea -like Oulophyllia sp. Platygyra sp. Pectinia sp. Trachyphyllia sp. Pavona sp. Millepora sp.

Ra Ra Ra Ra Ra/Co Ra Ra Ra Ra Ra/Co Ra Fr Co Ma Co Co Fm Pl Ra

95.5 121 2.5 0.5 5 25 0.5 0.5

39.5 53.5 5 0.5 2.5 0.5 0.5 0.5 21 26.5 12.5 2 13

47.5 19.5 0.5 0.5 5 7 0.5 0.5

139 23.5 6 3.5 13.5 3

73 10

14.5 37.5 5

11.5 3 2.5

28 2 0.5 2

14

409 265 19 5 81 36.5 1.5 1.5 21 182 18 80 20.5 27.5 132 4 74.5 1.5 1

29.6 19.2 1.4 0.4 5.9 2.6 0.1 0.1 1.5 13.2 1.3 5.8 1.5 2.0 9.6 0.3 5.4 0.1 0.1

Total

55 0.5 0.5

0.5 3.5 0.5 3

0.5

0.5 0.5

0.5 307

181.5

103

47

0.5 0.5

0.5 9.5 0.5

54.5 0.5

47 6 74 5.5 27 72 3.5 70

1 0.5 269.5

108.5

417

1380.5

Count of fragments Taxon

Form

NS50

NS51

NS52

NS53

NS54

Hand picked

Total

%

Dictyaraea sp.1 Dictyaraea sp.2 Dictyaraea micrantha Porites sp. Goniopora sp. Seriatopora irregularis Seriatopora hystrix Stylophora sp. Acropora sp. aspera group Alveopora sp. Montipora sp. Fungiidae sp. Leptastrea -like Oulophyllia sp. Platygyra sp. Pectinia sp. Trachyphyllia sp. Pavona sp. Millepora sp.

Ra Ra Ra Ra Ra/Co Ra Ra Ra Ra Ra/Co Ra Fr Co Ma Co Co Fm Pl Ra

309 134 7 6 9 108 4 1

189 123 14 45 13 10 10 5 52 20 38 13 2

108 16 4 1 3 11 2 1

317 25 16 24 1 12

136 8

11 17 3

2 4

11 4

21 7 6

31 5 3 4

13

21

6 2

9 2 2 2 2 11 2 6

1070 323 44 76 39 149 16 7 52 149 56 27 8 3 39 6 29 2 2

51.0 15.4 2.1 3.6 1.9 7.1 0.8 0.3 2.5 7.1 2.7 1.3 0.4 0.1 1.9 0.3 1.4 0.1 0.1

172

82

Total

55 6 2

1 1 5

4 15

1 1

1 646

554

184

However, it remains unresolved whether the observed difference is based on environmental parameters or is due to the time difference between early Miocene (Banyunganti) and late Miocene (TF 102) assemblages. This stresses the necessity for comparisons of assemblages from the same habitat when reconstructing biodiversity over time. To our knowledge, the TF 102 mollusk assemblage is at present the only detailed numerical analysis of a Neogene coral-associated mollusk assemblage from the region, so no comparisons with diversity from other coral-associated assemblages can be made. Quantitative data from comparable modern settings (e.g., Zuschin et al. 2001) were not available for comparison. These results emphasize first, the need for bulk samples rather than hand-picked samples, and second, the large sample sizes needed in hyperdiverse faunas. Ecological Variation between Environments The TF 102 mollusk assemblage is dominated both in taxon richness and in feeding guild abundance by predatory gastropods. The limited numerical

1

1 1 461

2097

data available suggest a similar pattern to that observed in modern tropical coral-associated mollusk assemblages. Taylor (1977, 1978) observed that the richness of predatory gastropods is highest in modern reef-associated gastropod assemblages compared to those from other shallow tropical marine environments in his study area at the Maldives. Because of the similarity of the applied sample processing and counting methods, the feeding guild composition of the TF 102 assemblage can be directly compared to the composition of the seagrass-associated Banyunganti assemblage (Fig. 6; Reich et al. 2014). The Banyunganti assemblage and the assemblage from TF 102 have a similar composition of feeding guilds when taxon richness is used. However, the feeding guild abundance data discriminate clearly between both environments, with the seagrass assemblage dominated by herbivores and the coral carpet assemblage by predators. Suspension feeders are less taxon-rich and abundant in the seagrass environment. A dominance of herbivorous and detritivorous gastropods is expected for seagrass-associated mollusk communities and has been used previously to

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FIG. 5.—Coral diversity at the TF 102 locality. A) Dictyaraea sp. 1, BMNH AZ6065. B) Dictyaraea sp. 2, BMNH AZ6035. C) Dictyaraea micrantha var. spinosa, BMNH AZ8797. D) Seriatopora irregularis, BMNH AZ8796. E) Alveopora polyacantha, BMNH AZ8788. F) Goniopora sp., BMNH AZ8790. G) Platygyra sp. AZ8786. H) Acropora sp. aspera group, BMNH AZ6006. I) Fungia sp., BMNH AZ8793.

identify seagrass meadows in the fossil record (Moulinier and Picard 1952; Davies 1970; Brasier 1975; Ivany et al. 1990; Reich et al. 2014). The comparatively low abundance and taxon richness of bivalves in the Banyunganti assemblage might be attributed to the presence of a dense rhizome mat that inhibited the establishment of an infauna (Davies 1970; James and Bone 2007). However, the majority of filter-feeding bivalves in the TF 102 assemblage is represented by epifaunal taxa, and it remains unknown why those taxa are rare to absent in the Banyunganti assemblage, although they are often common in modern seagrass associations (Mikkelsen et al. 1995; Reich et al. 2014). The data presented here may be applied for further studies on differences in feeding ecologies of mollusk assemblages from different habitats as a possible indicator for different paleohabitats. CONCLUSIONS

Our results indicate that in diverse tropical molluscan faunas it is essential to collect abundance data from large bulk sediment samples to be able to make standardized diversity estimates and ecological characterizations (e.g., Jackson et al. 1999). Furthermore, with over a thousand specimens counted, the rarefaction curve is not saturated, implying the need of even larger sample sizes in order to estimate species richness. When considered individually, the hand-picked samples yield far too few specimens to be useful in analyses. Another obstacle is that the

taxonomic impediment is huge. In the current assemblage we were able to identify only slightly more than 12% of the present taxa to species level, and several of these identifications remain uncertain. For paleoenvironmental reconstructions, characterizing a fauna by functional groups instead of a full taxon inventory yields much of the same information (Todd et al. 2002). The paleoenvironment of the upper Miocene TF 102 site from Bontang (East Kalimantan, Indonesia) can be interpreted as a coral carpet that developed in calm, shallow waters influenced by high inputs of finegrained sediments. Ramose corals of the extinct genus Dictyaraea were dominant in these settings and provided a suitable microhabitat for a diverse mollusk community. The mollusk assemblage associated with the TF 102 coral carpet is dominated in taxon richness and abundance by predatory gastropods. The proportion of taxon-based and abundancebased feeding guild composition in the studied coral carpet assemblage is very similar. A Miocene seagrass assemblage from the same region is typified by an increase in the proportion of the herbivore/detritivore guild in the abundance data when compared to the taxon data. Therefore, feeding guild composition of shallow marine tropical mollusk assemblages might yield a tool for the discrimination of paleohabitats in addition to sedimentological or other information, but a lot more data and further studies are required to determine the generality of the pattern. The coral-associated mollusk assemblage is more diverse than an early Miocene seagrass-associated assemblage from the same region; however,

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FIG. 6.—Comparison of mollusk feeding ecology using species richness (upper diagrams) and abundance data (lower diagrams) of the late Miocene coral carpet fauna from TF 102 (Bontang) and an early Miocene seagrass fauna from Bayunganti (Java; Reich et al. 2014). H 5 herbivores (including detritivores), CP 5 predatory carnivores, CB 5 browsing carnivores, S 5 suspension feeders, D 5 deposit-feeding bivalves, CD 5 chemosymbiotic deposit feeders. The specimen number for Bontang TF 102 is higher than reported in Table 1 as unidentified species of families were included in this analysis.

it is unknown if this is the result of variation in diversity over time or between different environments. This indicates the importance of carefully distinguishing paleohabitats in order to make meaningful comparisons of biodiversity. ACKNOWLEDGMENTS

This project is part of the Throughflow project (Marie Curie Initial Training Network: Grant No. 237922). In the field we were assisted by Professor Fauzie Hasibuan, Pak Aseb, Pak Untung, and Sonia Rijani (Pusat Survei Geologi Bandung). Vibor Novak (Naturalis, Leiden) made the TF 102 lithological column available. Charles Barnard (Naturalis) helped with sample processing. J. Darrell and L. Douglas assisted with the curation of coral specimens at the Natural History Museum, London (NHM), and we gratefully acknowledge the enthusiastic support of A. Thomas and the NHM ‘‘V-Factor’’ volunteers for exhaustive sample processing. We thank Jill Leonard-Pingel and an anonymous reviewer for their thoughtful comments. REFERENCES

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