Mollusc Shell Encrustation and Bioerosion Rates in a Modern ...

RESEARCH REPORTS 171

Copyright Q 2002, SEPM (Society for Sedimentary Geology) 0883-1351/01/0017-0171/$3.00

Mollusc Shell Encrustation and Bioerosion Rates in aModern Epeiric Sea: Taphonomy Experiments in the Java

Sea, Indonesia

HALARD L. LESCINSKYDepartment of Life and Earth Sciences, Otterbein College, Westerville, OH 43081

EVAN EDINGER* and MICHAEL J. RISKSchool of Geography and Geology, McMaster University, Hamilton, Ontario, L8S 4M1, Canada

PALAIOS, 2002, V. 17, p. 171–191

Mollusc shells of several species were deployed on racks andon the seafloor for up to two years on eutrophic and mesotro-phic reefs in the Java Sea, a modern epeiric sea. Taphonom-ic indicators of shell preservation decreased during thestudy, but some ligament, periostracum, and shell color per-sisted throughout. Shell fragmentation was negligible ex-cept for species with easily chipped margins; weight losswas less than 5% for sturdy shells and up to 15% for shellswith chipped margins. Shells deployed in mesh bags on thesediment surface had low encrustation and bioerosion,probably because of partial or complete burial. Areal en-crustation on shells in bags was greater at the mesotrophicsite than the eutrophic site, but animal encrustation andbiovolume of encrusters was greater at the eutrophic site.

Shells elevated on racks were encrusted rapidly at allsites; animal encrustation rates were correlated positivelywith productivity, and biovolume of encrusters was greateron nearshore eutrophic reefs than on offshore mesotrophicreefs. Bioerosion rates were variable but also tended to behigher at the more productive site. Natural shells also ex-hibited a positive, though less strong correlation with pro-ductivity suggesting that encrustation intensity and shellbioerosion may serve as relative indicators of productivityin the fossil record.

INTRODUCTION

Although the fate of shells in natural environments isessential to our understanding of fossilization, most actu-alistic studies of shell taphonomy have been limited to in-tertidal and very shallow subtidal environments wherefossilization potential is generally low (e.g.; Driscoll, 1970;Peterson, 1976; Flessa et al., 1993; Meldahl et al., 1997).Only recently have studies begun to focus on environ-ments where most fossil shells are preserved: shallow ree-fal, mixed carbonate-siliciclastic, and shelf-depth muddyenvironments (e.g., Parsons et al., 1997, 1999; Walker etal., 1998; Best and Kidwell, 2000a, b). This study exam-ines encrustation and bioerosion patterns on shells in amodern epeiric sea—the Java Sea. The Java Sea, on the

* Present address: Departments of Geography and Biology, MemorialUniversity of Newfoundland, St. John’s, Newfoundland, A1B 3X9,Can-ada

southern portion of the Sunda Shelf (Tjia, 1980) is one ofthe modern world’s only epeiric seas, and may serve as ananalogue for understanding ecologic and taphonomic pro-cesses that occurred over large areas of the continents dur-ing the early and middle Paleozoic (Edinger and Risk,1998; Edinger and Browne, 2000; Edinger et al., 2000a).

Sites in the Java Sea represent opposite ends of a gra-dient in burial and planktonic productivity. Recent tapho-nomic studies (e.g., Walker et al. 1998; Parsons et al.,1999; Best and Kidwell, 2000a) suggest that burial andproductivity within the water column are generally thetwo most important environmental factors controlling therelative importance of accretionary and destructive taph-onomic processes. This study examines how rates of en-crustation and bioerosion are related to planktonic pro-ductivity and burial, and how these variables can be usedto predict whether bioaccumulation or bioerosion predom-inate (Walker et al., 1998). The study also addresses thehypothesis that encrustation levels and bioerosion inten-sity may be useful indicators of paleoproductivity in fossildeposits (Lescinsky and Vermeij, 1995; Edinger and Risk,1997).

Encrustation Rates and Productivity

Planktonic productivity is the ultimate food source forsuspension feeding epibionts (encrusters) and endobionts(borers) and, hence, most processes of encrustation andbioerosion are positively correlated with primary produc-tivity. The importance of productivity on benthic encrus-tation has been demonstrated best by studies of ‘‘fouling’’on artificial settling plates (e.g., cement or ceramic tiles).Birkeland (1977, 1989) found that encrustation in a vari-ety of habitats was correlated positively with planktonicproductivity and that in many environments surfaces canbe nearly covered within a year. Anthropogenic enrich-ment (pollution) can cause similar effects (e.g., Moran andGrant, 1989).

On natural shells, encrustation rates in general, and theeffect of productivity in specific, are less well known.Voight and Walker (1995) found that deep sea gastropodshells were encrusted more heavily in productive watersthan elsewhere, but the effects of environmental variableson encrustation are just beginning to be explored. TheShelf and Slope Experimental Taphonomy Initiative(SSETI—Parsons et al., 1997, 1999; Walker et al., 1998)will provide a framework for examining encrustation

172 LESCINSKY ET AL.

along depth gradients in carbonate (Bahamas, to 267m)and siliciclastic (Gulf of Mexico to 607m) facies. The pre-sent study in the Java Sea provides a framework for un-derstanding similar processes in shallow epeiric sea envi-ronments.

Shell Bioerosion Rates and Productivity

Several studies have shown that rates of internal bioe-rosion are correlated with planktonic productivity for coralsubstrates in reef environments (Risk and MacGeachy,1978; Highsmith, 1980; Sammarco and Risk, 1990; Edin-ger and Risk, 1997; Pandolfi and Greenstein, 1997), butlittle work has examined bioerosion rates on molluscshells or in shallow muddy bottom facies. The best empir-ical data on bioerosion rates of carbonate skeletons arefrom Kiene and Hutchings (1992, 1994) who found that ina variety of reef environments, seven- and nine-year oldcoral pieces had rates of carbonate loss of 2–2.5 kg/m2/y(patch reef and lagoon) to 0.35–0.46 kg/m2/y (reef flat anddeep leeward) on the Great Barrier Reef. Similarly highrates have been documented at other reefs (Chazottes etal., 1995, Pari et al., 1998). Most of this bioerosion is theresult of surficial scraping during grazing by echinoids(Bak, 1990, 1994; Mokady et al., 1996), parrot fish (Bell-wood, 1995), and chitons (Rasmussen and Frankenberg,1990), particularly in the early stages of bioerosion (Cha-zottes et al., 1995). Macroboring intensity is initially verylow and is often an order of magnitude less than grazing(Pari et al., 1998), but increases in importance with expo-sure time (Bromley et al., 1990).

Observed bioerosion rates on coral are equivalent to theloss of approximately 1 mm of thickness (per exposed sur-face) each year. If bioerosion on shells proceeded at similarrates, shells that are only several mm thick would be de-stroyed in a single year or two, especially if eroded on bothinterior and exterior surfaces (Edinger, 2001). The pres-ence of shell beds and a fossil record, therefore, requiresthat shells (where fossilized) have much lower bioerosionrates than those documented on experimental coral sub-strates.

Rates of molluscan shell breakdown are poorly knownfor most modern environments. Algal and fungal boringsare common in shells (Akpan and Farrow, 1985; Radtke,1993; Cutler, 1995), and sand-sized molluscan shell frag-ments in a reef lagoon lost about 3 percent of weight peryear principally to microboring algae (Tudhope and Risk,1985). Conversely, Driscoll (1970) and Walker et al. (1998)found that experimentally deployed shells actually gainedweight from attached epifauna during the first year ormore of exposure. Subsequent shell weights decreased asmacroborings increased. This follows the general patternof slow initial colonization by macroborers during the first1–2 years (Bromley and d’Alessandro, 1990; Bromley etal., 1990; Peyrot-Clausade et al., 1992; Walker et al., 1998)in most environments.

Dissolution of exposed and buried shells also is an im-portant process that may destroy thin shells prior to fos-silization (Davies et al., 1989). Shell dissolution largely isdetermined by the chemistry of sediment pore waters, andby the structure and composition of the shells. Aragoniticshells in cold, slightly acidic pore waters are more prone todissolution than are dominantly calcitic shells in warmer

or more alkaline pore waters. These patterns in pore-wa-ter chemistry are controlled largely by temperature, sedi-ment composition, and organic content (Walker and Gold-stein, 1999; Best and Kidwell, 2000a).

Effects of Burial

Burial prevents recruitment of epibionts and endo-bionts, and stops suspension feeding by establishedbionts;therefore such activity limits encrustation and bioerosionalthough some algal and fungal microborings and disso-lution may persist in the upper layers of sediment (Radt-ke, 1993). The importance of burial can be seen easily, forexample, on modern scallops living on soft bottoms.Whereas live mobile scallops can shed sediment and sup-port rich epibiont assemblages, rapid burial of emptyshells results in little post mortem encrustation of shell in-teriors, and little encrustation of co-occurring infaunal bi-valve shells (Lescinsky, 1993). Similar patterns have beenobserved on the Bahama platform (Parsons et al., 1999)suggesting that most examples of encrustation in the fos-sil record may reflect settlement on live hosts or of shellsresting on hard or firm bottoms, rather than encrustationof shells in soupy muds (Lescinsky, 1995; Parsons et al.,1997, 1999; Walker et al., 1998; Best and Kidwell, 2000a).

Burial of shells results from net sedimentation, sedi-ment resuspension during storms, or by bioturbation.Thus, shells on muddy bottoms may be covered quicklywith a thin layer of sediment, even in the absence of posi-tive sedimentation (Parsons et al., 1999). Resuspension ofsediments is likely to have been important in most epeiricseas (Johnson, 1987). For example, in nearshore environ-ments of the Java Sea, sediment resuspension reduces wa-ter clarity to near zero during the stormy winter months(Edinger et al., 1998, 2000a); deployment of the experi-mental shells for this study produced the same effect (seemethods, below).

Episodic exhumation during storms or via bioturbationcan reintroduce shells into the taphonomically active zone(TAZ, Davies et al., 1989) making exhumation a compli-cating factor in understanding taphonomic history in en-vironments such as carbonate sands (Meldahl et al., 1997;Kowalewski et al., 1998). In other environments, stormsprimarily resuspend mud that later settles and burieslarge bioclasts. In these environments, exhumation is lesscommon and attributed to bioturbation, mobility of live or-ganisms, and for gastropod shells, reoccupation by hermitcrabs (Walker, 1989; Walker et al., 1998). Burial ratherthan exhumation appears to be the rule in the muddy en-vironments of the Java sea; few bioclasts are visible nearthe sediment water interface and dredging of surficialmuds by local fishermen yields few dead mollusc shells.

METHODS

Study Area: The Java Sea

The Java Sea lies on the Sunda Shelf and is less than100 m deep throughout (Fig. 1). It has been exposed peri-odically during sea-level lowstands, and drowned Pleisto-cene river channels indicate that it was drained entirelyduring Pleistocene glaciations (Tjia, 1980). The Java Seare-flooded approximately 10–12,000 ybp with seas attain-

JAVA SEA TAPHONOMY 173

FIGURE 1—Study sites in the epeiric Java Sea include 3 sites in theoffshore Karimunjawa Islands (Gosong Cemara, Batu Lawang, andLagun Marican) and 3 sites adjacent to Java (Pulau Panjang, TelukAwur- fossil reef, and Semarang Harbor).

ing modern levels by 7000 ybp (Hanebuth et al., 2000).Circulation is dominated by seasonal monsoons (Wyrtki,1961), as were some ancient epeiric seas (e.g., Marsagliaand Klein, 1983). During the east monsoon (May–Octo-ber), conditions are generally dry and stable and waterturbidity is low; stormy west monsoon conditions resus-pend sediments and increase mud sedimentation from riv-ers (Hoekstra, 1993), making field work difficult. Rates ofsediment delivery to the shallow seas of Southeast Asiaare among the highest in the modern oceans (Millimanand Meade, 1983). Although Java Sea sedimentation maybe high, in part, because of recent deforestation, the steepandesitic rocks of Java naturally weather quickly intoclays, and sediment cores record high rates of mud depo-sition throughout the Holocene (Tjia, 1980; Dewi, 1997).

Sea-surface temperatures range between 25 and 28oC;average surface salinity is 32 ppt in the wet season and 33ppt in the dry season (Wyrtki, 1961). The Java Sea has thehighest primary productivity of the Indonesian seas (Po-lunin, 1983). The euphotic layer is ,50 m deep, and wa-ters are generally mesotrophic, with locally eutrophic en-vironments nearshore, and hypertrophic conditions in ar-eas subject to organic pollution (Edinger et al., 2000b).Coastal phytoplankton biomass concentrations in the wetseason are typically double those of the dry season (Polun-in, 1983).

Java Sea sediments are dominated by siliciclastic mud(up to 98% silt and clay; De Wilde et al., 1989) derived

from the volcanic highlands of Java. Surficial muds arenot generally anoxic, but do contain significant amounts oforganic matter (Dewi, 1997). Offshore soft fluid muds sup-port a depauperate macrofauna including a solitary cupcoral (Flabellum) and the molluscs Spondylum wrighti-anus and Stellaria solaris, all with flotation spines (DeWilde et al., 1989). Nearshore siliciclastic muds aroundSemarang support a local mollusc fishery for Anadara in-flata, Anadara granosa, Placuna, Paphia, Babylonia (Fig.2), and other shellfish. Scattered patch and platform reefswithin the Java Sea include eutrophic nearshore reefs andoffshore mesotrophic to oligotrophic reefs.

Study sites (Table 1, Fig. 1) include a range of sedimenttypes and productivity levels (measured as Chlorophyll Avalues). Pulau Panjang is a nearshore coral cay, withabout 80% carbonate content, subject to anthropogenic eu-trophication from sewage, agricultural runoff, and aqua-cultural effluent (Edinger et al., 1998; Heikoop et al.,2000). Three study sites are in or adjacent to the Karimun-jawa Islands National Marine Park: an offshore coral cay(Gosong Cemara), a mangrove fringing reef and adjacentcarbonate mud (Lagun Maricun), and a back reef lagoon(Batu Lawang). Carbonate sediments dominate most fa-cies around the Karimunjawa islands; however, siliciclas-tic sediments derived from Pliocene basalt flows and ar-kosic sandstones also are found in the mangrove fringingreef (Edinger et al., 2000a). Experiments were deployed atthe leeward edges of nearshore and offshore coral cays(Pulau Panjang and Gosong Cemara; Fig. 1). Concrete set-tling tiles for a related study were deployed at leeward andwindward edges of the cays and at the mangrove fringingreef (L. Marican).

Fossil shells were collected from a small (1.5–3m expo-sure) Holocene reef at Teluk Awur near Panjang. The reefdates to approximately 7000 ybp (Edinger et al., 1996a)during the Holocene hypsithermal when sea levels brieflyexceeded modern sea levels. The subfossil reef preservesprimarily reef-flat facies, and consists of two horizons ofupright Porites microatolls. The corals are covered and in-filled by a 30–50cm layer of coral and mollusc rudstone.The subfossil reef is similar in coral composition to the Pu-lau Panjang reef flat, and is considered a pre-pollution an-alogue to it (Edinger et al., 2000c).

Experimental Design

Four types of samples were considered in this study: ex-perimental shells deployed on racks above the seafloor, ex-perimental shells deployed in bags on the seafloor, naturalshells found exposed on the seafloor, and subfossil shells.Rack and shell-bag experiments were designed to be com-parable to those of SSETI (e.g., Parsons et al., 1997, 1999;Walker et al., 1998). All experimental shells (Table 2, Fig.2), except Striostrea, were live collected by Semarang fish-ermen using small dredges on fluid muds and were airdried to remove soft parts. Ligaments of A. inflata, A. gra-nosa, and Paphia were cut to disarticulate valves, butwere not removed prior to deployment. Any adherent or-ganisms were removed and shells with macroborings wereexcluded from the study. Striostrea valves were collectedfrom refuse piles of recent, yet indeterminate, age adja-cent to the mangrove-dominated shoreline where they hadbeen harvested for food.


FIGURE 2—Molluscs used in the experiments. (A) Babylonia pallida, (B) Placuna placenta, (C) Anadara inflata, (D) Anadara granosa, (E)Striostrea sp., and (F) Paphia undulata. Placuna is 9 cm across.

Rack Experiments

Shells of two bivalve species (Anadara inflata and Pla-cuna placenta) were drilled and then fastened with plasticcable ties to racks of PVC pipe approximately 0.5 metersabove the seafloor. Racks were deployed at the base of thereef at Panjang (6m) and at Cemara (10m). The racks alsoheld coral slabs, concrete tiles, and other substrates, aspart of a larger study on coral recruitment to artificial reefmaterials (Edinger et al., 1996b). Three racks were de-ployed adjacent to each other at the edge of the reef. Thisdesign permitted 3 sampling intervals of 3 shells at 3month, 6 month, and 1 year intervals. Individual shellsconstituted replicates. Unfortunately, racks at Cemarawere vandalized and lost prior to the 1 year collection (Ta-ble 2).

Concrete settlement tiles deployed as part of anotherstudy (Edinger et al., 1996b) also were incorporated intothis study to add additional data when examining pat-terns of encrustation and productivity. Sites for concretetiles included both Panjang and Cemara sites, the wind-ward sides of Pulau Panjang (6m) and Gosong Cemara

(10m), and the base of a fringing reef within mangroves,Lagun Marican (3m).

Bag Experiments

Experimental shells of six species (Fig. 2, Table 2,3)were deployed directly onto the seafloor in 1-cm meshnylon bags adjacent to the rack experiments at 10mdepth at Panjang (nearshore eutrophic) and Cemara(offshore mesotrophic) reefs. The five bivalves (Anadarainflata, A. granosa, Paphia undulata, Placuna placenta,and Striostrea sp.) and one gastropod (Babylonia canal-iculata) were chosen because they were readily avail-able from Semarang fishermen and reflect a range ofskeletal microstructures and shell thicknesses (Table3). Bivalves were emphasized over gastropods becauseof local availability and to more closely approximate themorphological composition of brachiopod-dominatedPaleozoic epeiric sea faunas. Mesh bags were largeenough that shells did not touch each other during de-ployment, but evidently shells shifted during the exper-


TABLE 1—Description and physical characteristics of study sites. Physical data for experimental sites include Chlorophyll A (productivity),suspended particulate matter (SPM), organic and carbonate components of sediment, and sediment resuspension rates. A complete set ofenvironmental measurements was not available for sites where natural shells were collected.

SiteNum-

ber Site name Locality descriptionDepth

(m) Substrate

Chl. A(mg/m3) SPM

% Or-ganic

%Car-bon-ate

Resu-spended

sedi-ment;

mg/cm2/day

Experimentaltreatments

1a Panjang 1

Eutrophic site at the base ofthe nearshore patch reef,south (leeward) side of Pu-lau Panjang island, near Je-para, Central Java. 6

coral rubble, car-bonate sandand silt 1.09 28.9 7.8 74.1 27.1

Elevated shells,natural shells,cement tiles

1b Panjang 2

Eutrophic site 10 m south ofSite 1, in slightly deeperwater, with muddier bottom 10

soft silty bottom,and some coralrubble — — — — — Shell-bags

2 Cemara

Mesotrophic site at the southedge (leeward) of GosongCemara patch reef, Kari-munjawa Islands, CentralJava Sea 10

Coral, coral rub-ble 0.25 20.3 2.3 99.3 4.1

Elevated shells,shell-bags, nat-ural shells, ce-ment tiles

3Lagun Mari-

can

Eutrophic patch reef at en-trance to mangrove bay(Lagun Marican), Karimun-jawa Islands 3 carbonate mud 1.24 26.39 11.2 81.7 —

natural shells,cement tiles

4 Batu Lawang

Mesotrophic semi-protectedshallow bay (Batu lawang),Karimunjawa Islands 1 Carbonate sand — — — — — natural shells

5 Semarang

Semarang Harbor, adjacent tothe city of Semarang, Cen-tral Java 3

soft siliciclasticmuds — — — — — natural shells

6 Taluk Awur

Holocene subfossil exposure, 3m thick, along shore, ap-proximately 5 km south ofJepara at the village of Ta-luk Awur

carbonate sandaround patchreef of coralmicro-atolls — — — — — fossil shells

TABLE 2—Actual sampling intervals and number of specimens for rack and bag experiments.

Taxa

Panjang (eutrophic)

Number ofspecimens

recovered persampling interval Sampling intervals

Cemara (mesotrophic)

Number of specimensper interval Sampling intervals

Elevated RacksAnadara inflataPlacuna placenta

33

3m, 6m, 1yr3m, 6m, 1yr

33

3m, 6m3m, 6m

Shell BagsAnadara inflataAnadara granosaPlacuna placentaBabylonia canaliculataPaphia (paphia) undulataStriostrea sp.

303030303030

3m, 6m, 1yr3m, 6m, 1yr3m, 6m, 1yr3m, 6m, 1yr3m, 6m, 1yr3m, 6m, 1yr

303030303030*

6m, 1yr, 2yr6m, 1yr, 2yr6m, 1yr, 2yr6m, 1yr, 2yr6m, 1yr, 2yr6m, 1yr, 2yr

Note: Cemara racks were lost prior to the one year retrieval, and only 20 specimens/species were retrieved at Cemara at 2 years.

iment and some shells were lying on or against otherswhen recollected. Bags were tethered to cinder blocks toaid in retrieval. Each shell bag contained preweighedlots of 10 valves of each of the six mollusc species.Twelve bags were deployed at each of the two localitiesand were retrieved (three at a time) at the same inter-vals at which rack experiments were collected (Table 2).

Individual valves were treated as replicates for all taph-onomic characters except weight loss, allowing 30 repli-cate shells per species per sampling interval. Preweigh-ed lots of 10 valves constituted replicates for weightloss, allowing 3 replicate measures of weight loss perspecies per sampling interval, except for the 2 year Ce-mara interval when only 2 bags were retrieved.


TABLE 3—Characteristics of mollusc shells deployed in experiments.

NameLength(mm)

Area(mm2)

Thickness(mm) Periostracum Unaltered color Shell structure

Anadara inflataA. granosaPlacuna placentaPaphia textileBabylonia caniculataStriostrea sp.

542290304460

270600

64001200800

1700

1.71.50.51.20.91.3

brown, hairybrown, smoothnoneclear, smoothclear, smoothnone

whitewhitewhite, translucentyellow, patternedbrown, mottledwhite and purple

aragonite, cross lamellararagonite, cross lamellararagonite, cross lamellar, flexible, high organicsaragonite, cross lamellararagonite, nacreous, cross lamellarcalcite, prismatic

TABLE 4—Composition of ‘‘natural shell’’ collections at various sites. All shells were collected dead except for Semarang Placuna. Taxaidentified using Roberts et al. (1982).

Site Guild Species N Total N

1 Panjang

2 Cemara

infaunalepifaunal-sessile

infaunal

Periglypta purpureaAnadara maculosaBarbatia helblingiiAcrosterigm subrugosaGafrarium divaricata

30171364

3030

22

Glossus moltkianaPeriglypta reticulataTapes literataPitar manillaePeriglypta purpurea

43111

epifaunal-vagileunidentifiableChlamys senatoriaLima (ctenoides) annulataPecten tigrisLima vulgaris

212754

29

3 Marican

4 Batu Lawang5 Semarang

epifaunal-byssalepifaunal-byssalinfaunalepifaunal-free lying

Lima fragilisSeptifer bilocularisBarbatia fuscaAcrosterigm subrugosaPlacuna placenta (live)

121353521

21353521

6 Taluk Awur

hermitted

fossil infaunalfossil infaunal

Turritella terebraFusinus sp.Murex acanthostephesNatica vitellusAcrosterigm subrugosaGafrarium pectinatum

10632

3235

21

3235

Natural Shells

Naturally occurring bivalve shells were collected adja-cent to the two experimental sites (Panjang and Cemara),at the back reef lagoon (Batu Lawang), the base of themangrove fringing reef (L. Marican), and from dredgehauls near Semarang (Table 4). Shells visible on the sur-face and more than 75 percent intact were hand-collectedusing SCUBA or snorkel. Collections exhibited a mixtureof apparently recently dead shells (still articulated with notaphonomic alteration) and older shells.

Fossil Shells

Single valves of two bivalves (Table 4) were collectedfrom the coral and mollusc rudstone at Taluk Awur. Therudstone overlies and infills around the coral microatolls,and is interpreted as a shallow reef and peri-reefal stormdeposit that had minimal reworking on the reef flat (Edin-ger et al., 1996a). Shells mainly were disarticulated, im-bricated, and oriented convex-up.

Environmental Variables

Chlorophyll A content, suspended particulate matter(SPM), and sediment composition were measured usingstandard methodology at Panjang, Cemara, and Marican(Burnison, 1980; Parsons et al., 1984; Edinger et al.,2000b). Chlorophyll A values (reported in Edinger et al.,1998, 2000b) were collected as a proxy for planktonic pro-ductivity because the preferred measure of organic carbonflux (Nixon, 1995) was logistically not possible. Reefs wereclassified as oligo-, meso-, eu-, or hyper-trophic accordingto Bell (1992) and Edinger et al. (2000b).

Sediments were sampled by taking replicate surfacegrabs from each reef adjacent to the experimental sites.Sediment samples were analyzed for carbonate composi-tion and organic content. Organic content of sedimentswas determined by weight loss after hydrogen peroxide di-gestion. Thirty percent H2O2 was added to sediments to di-gest organics, the supernatant was decanted off, and theremainder was dried and weighed. Sediment resuspen-


TABLE 5—Semi-quantitative taphonomic attributes examined in thestudy (modified from Davies et al., 1990).

Fragmentation1 Whole2 .90% intact3 81–90% intact4 61–80% intact5 ,60% intact

Carbonate Precipitation1 Original shell surface2 Patchy carbonate crust3 Continuous carbonate crust

Dissolution1 No dissolution2 Minor (,25%) pitting, chalkiness3 Major dissolution

Color1 Original2 Original, but dulled3 Loss of color (white)

Mineral Staining1 Original color2 Discolored (red/brown/black)

Periostracum1 Original2 Partially removed3 Periostracum absent

Ligament1 Full (cut for deployment)2 Partially removed3 Ligament absent

sion rate was measured at Panjang and Cemara usingsediment traps (Edinger et al., 2000a).

Data Analysis

Type and Percent Cover of Boring and EncrustingOrganisms

Percent cover of boring and encrusting organisms on el-evated shells was recorded in the lab as a proportion of theareal cover using point counts of a 1cm grid drawn on anacetate sheet. The sheet was flexed over the convex surfac-es of shells to minimize 3-dimensional distortion. Boringintensity was checked by sawing A. inflata shells medially,from beak to margin with a rock saw, and measuring thepercentage of the cross sectional area shell material thathad been removed. Areal percent cover for shells frombags, natural shells, and fossil shells were estimated tonearest 10% for coralline cover, animal cover, and boringintensity while viewing through a dissecting microscope.Epibiontic taxa were identified to taxonomic groups(sponges, cheilostome bryozoan, cyclostome bryozoan, cal-careous algae, fleshy algae, barnacles, oysters, Chama,disciniscid brachiopods, foraminifera, serpulid and spiror-bid polychaetes, and coral spat). Examples of A. inflataand P. placenta from elevated racks and sediment-surfaceshell bags at both experimental sites were subsampledwith scanning electron microscopy to examine microbor-ing and dissolution.

Areal cover of epibionts was compared among sites,treatments, and taxa using 1-way ANOVA, after checkingfor normality and homogeneity of variance. Degree of ma-croboring was compared among sites and treatments intwo ways. First, the frequency of bored shells at each siteand treatment was compared using 2-tailed t-tests assum-ing unequal variance. The rate of increase in frequency ofbored shells was determined as the slope of the log-trans-formed curve of duration of exposure versus percentage ofshells bored. Significance of differences between rates wasassessed by comparing regression co-efficients using an F-test (Sokal and Rohlf, 1981). Next, the area of each shellaffected by macroborers for those shells that were bored(i.e., non-zero values) was compared among sites andtreatments using 2-tailed t-tests assuming unequal vari-ance. Data were log-transformed to homogenize variance,as necessary. Because the frequency of infestation by ma-croborers increased through time, sample numbers ofbored shells increased through time.

Taphonomic Indicators

Taphonomic indicators of shells were scored using thesemi-quantitative framework of Davies et al. (1990) withminor modifications (Table 5). Mineral staining of shells(discoloration of Davies et al., 1990) was separated fromcolor loss because it results from different processes, suchas bacterially-mediated oxide precipitation in low oxygenpore water during burial (Raghukumar et al., 1989; Walk-er and Goldstein, 1999). For measurements of shell color,staining, periostracum, dissolution, and precipitation, bi-valve-shell surfaces were divided into eight external andeight internal shell regions; gastropods were divided intofive regions and each shell region was scored independent-

ly. Because shell regions differed in size, the score for eachshell was determined by summing the shell regions ac-cording to their proportion of the total surface area.

Weight-loss data for each species was computed by com-paring pre-deployment and post-retrieval weights for eachspecies (10 shells) in each shell bag retrieved per samplinginterval (usually 3 bags per interval). Weights of individ-ual shells were not recorded.

RESULTS

Physical Variables

The two experimental sites, Panjang and Cemara, differgreatly in substrate and productivity (Table 1). Panjang,the near-shore site was eutrophic (Chlorophyll A 5 1.09mg/m3), had a high organic sediment content (7.8%), andcontained 18.1% non-carbonate mud. Cemara, in the cen-tral Java Sea was mesotrophic (Chlorophyll A 5 0.25 mg/m3), had low organic content (2.3%), and sediment was99.3% carbonate. Resuspension of sediments was alsovastly greater at Panjang than Cemara (27.1 vs. 4.1 mg/cm2/day) which was reflected in the condition of the bagswhen retrieved. Bags at Panjang were buried under 1–2cm of mud after 1 year; Cemara bags were covered onlypartly by a veneer of carbonate sand.

Encrustation

Elevated shells were encrusted rapidly at both Panjangand Cemara (Fig. 3A,B) with highest rates (near 100 per-cent cover after 6 months) in the eutrophic waters. Higherencrustation at Panjang is significant at 3 months (t(12,12) 5


FIGURE 3—Total encrustation of experimental shells comparing eu-trophic (A,C) and mesotrophic (B, D) environments, and elevated(A,B) and seafloor (C,D) treatments. Areal cover of encrusters isshown through time for four surfaces, Placuna, Anadara inflata shellinteriors and exteriors, and cement tiles. Tiles from the same locationsare included because vandelism prematurely ended the Cemara rackexperiment prior to one year. Encrustation was greatest on elevatedsubstrates at the eutrophic reef (A), where cover approached 100 per-cent on concave shell interiors after 6 months. Shells on the seafloor(C,D) were sparsely encrusted, particularly at Panjang (C) where theybecame mud covered.

FIGURE 4—Composition of encrusting biotas on elevated shells. Atthe eutrophic site (A,C,E) a high percentage of shell-surface area wascovered by large encrusters, such as barnacles, bivalves, and spong-es (common after 1 year). Fleshy algae was common as ‘‘other.’’ Themesotrophic site (B,D,E) was dominated by bryozoans and ‘‘other’’(mostly coralline algae and calcareous annelids). Ecological succes-sion at Panjang is represented by increasing sponge cover and de-creasing bryozoan cover through time. Type of shell surface (Placuna,A. inflata interiors and exteriors) was less important than experimentalsite in determing encruster biota.

2.80, p , 0.01) and at 6 months (t(11,12) 5 1.77, p 5 0.05)when elevated substrates are considered together.

Taxa of encrusters differed between the two sites (Fig. 4,5). At the eutrophic Panjang site, bryozoans, barnacles, bi-valves, and sponges were most common. At the mesotro-phic Cemara site, bryozoans, were most common, barna-cles were absent, and bivalves were significantly less com-mon (t(9,9) 5 4.14, p , 0.01). Serpulid worms and corallineand fleshy algae (grouped together as ‘‘other’’, Fig. 4) werecommon at the mesotrophic but not the eutrophic site.

Individual encrusters were larger at the eutrophic site;oysters up to 3.5 cm and barnacles to 2.2 cm were recordedafter 6 months. Large sponges had overgrown some oys-ters, barnacles, and other encrusters after a year (e.g., Fig.5D). After 6 months at the mesotrophic site, the largest en-crusting oyster was only 0.9 cm.

Shells on the seafloor (bag experiments) had much low-er encrustation than elevated shells, with less than 2.2percent cover on shells deployed on eutrophic muds afterone year (Fig. 3C, D; Appendix). Low encrustation proba-bly resulted from burial in the mud, as bags retrieved after6 months and 1 year were partially to completely buried in1 to 2-cm of mud. A few bivalves colonized the bags them-selves during the study including an attached Pinctada(4.5 cm long) and an infaunal Placemen tiara (3.5 cm long).

Shells on the seafloor at the mesotrophic site (Cemara)were not buried, but were dusted with carbonate sand.These shells had greater encrustation (Figure 3D) thanshells from the eutrophic site after 6 months (1-way AN-OVA, F 5 9.81, p , 0.01) and 1 year (F 5 40.7, p 5 0.023).After 2 years, some shell types at the mesotrophic site av-eraged up to 12% cover, primarily of serpulids and coral-line algae with a variety of other less common encrustersincluding foraminiferans and disciniscid brachiopods.

Differences in encrustation among the six experimental


FIGURE 5—Examples of A. inflata from rack and bag experiments, and natural shells. (A-D) Panjang elevated shells, A. 3 months, B. 6 months,C. and D. 12 months. (E-G) Cemara elevated shells, E. 3 months, F. and G. 6 months. (H) Cemara Natural shell. (I-K) Panjang bag shells, I.3 months, J. 6 months, K. 12 months. (L) Panjang Natural shell. (M-P) Cemara, bag shells, M. and N. 6 months, O. 12 months, P. 2 years.Note that elevated shells from the eutrophic reef (A-D) are encrusted more heavily than mesotrophic examples (E-G). Eutrophic encrustersinclude barnacles (b), sponges (s), and oysters (o). Oyster in B has been successfully drilled by a muricid gastropod. Encrusters on mesotrophicexamples include serpulid annelids (a), fleshy algae (f), and rare corals (c). Bag shells (I-K, M-P) have little encrustation or alteration. Naturalshells (H and L) have intermediate amounts of encrustation and alteration.

mollusc species deployed in the mud (Fig. 6) apparently arerelated, in part, to size. The smallest species (A. granosa)had the lowest percent cover while the larger species (A. in-flata, Placuna, Babylonia, Striostrea) were encrusted moreheavily at mesotrophic and eutrophic sites. Among the larg-er species, however, size was not crucial; Striostrea had thehighest encrustation although Placuna was larger.

Differences in encrustation also were apparent betweenconcave shell interior surfaces and convex shell exteriors(Fig. 6,7). On both elevated and bottom shells, initial colo-nization (3–6 months) was greater on concave surfaces. Af-ter 12–24 months encrustation on convex surfaces ap-proached, and in some cases surpassed, encrustation on theconcave interiors (ratio of interior/exterior encrustation,1). Flatter species (e.g., Placuna, Paphia; Fig. 6) had lessdisparity between valve surfaces than more convex species.

Naturally occurring shells had encrustation rates inter-mediate between elevated and bottom experimentalshells; generally around 20% of external shell surfaceswere covered (Fig. 8). Animal encrusters predominated atthe Semarang and Panjang eutrophic sites while algal en-crusters were most common at the mesotrophic sites. Anexception was the eutrophic mangrove site, Marican,where coralline algae was most abundant. This site wasvery shallow (0–3 meters); only shells of two bysally at-tached bivalve species were found, and these were collect-ed on rubble of the small fringing reef. The bivalves wereencrusted while alive on upright hydroids and corals, andmost empty shells appeared to result from recent preda-tion. No shells were visible on the soupy carbonate mudsadjacent to the reef.

Hermitted gastropod shells illustrate how a mobile host


FIGURE 6—Encrustation of six species of mollusc shells on the sea-floor 6 months and one year after deployment. Panjang (eutrophic)shells had low total cover (2–5%) while Cemara (mesotrophic) shellshad higher encrustation (3–25%). Encrustation intensity was not gen-erally correlated with shell size, although A. granosa, the smallest spe-cies, also had the least encrustation.

FIGURE 7—Relative encrustation on concave and convex surfaces. Concave surfaces were encrusted about twice as heavily as convexsurfaces 6 months after deployment in shells on sediment (A) and elevated (B). By 1 year, intensities were similar or convex surfaces wereencrusted more heavily. Encrustation of shells on the sediment at Panjang was too low for meaningful ratios.

facilitates encrustation in mud (Figs. 8,9). Several Baby-lonia in the bag experiments became occupied by crabsduring the study and had high levels of encrustation. Like-wise, Turritella and other gastropod shells collected infisherman’s dredges in siliciclastic muds in SemarangHarbor rarely were encrusted, unless hermitted. Hermit-ted shells there had about three times the cover of the liv-ing epifaunal bivalve Placuna (Fig. 8).

Fossil shells had few encrusters (Fig. 8). Some shell sur-faces were chalky and corroded, and may have held coral-line algae, but distinguishing fossil algal cover was impos-sible. Recognizable encrustation was limited to 1% and 3%of the interior surfaces of venerids (Gafrarium) and cock-les (Acrosterigm), respectively (Fig. 8).

Bioerosion

Bioerosion rates were examined using two measures:macroborings and weight loss. Macroborings were not ob-served at all on elevated shells during the experiments,and shells on the seafloor at both sites showed little initialsign of borings. Only one shell (of 180, Table 2) was boredafter 3 months at Panjang and there were still few boringsafter 6 months (Fig. 10A). The proportion of bored shellsincreased through time at both sites, yet most shells re-mained unbored for the duration of the study (Fig. 10A).The maximum observed frequency of boring was 23% ofshells after 2 years at Cemara.

The average rate of increase in Cliona infestation ofshells was determined as the slope of the log-transformedcurve of duration versus percentage of shells infested. Theaverage rate of increase in Cliona infestation of shells was11% per year at Panjang, and 5% per year at Cemara.These rates were significantly different (Fs 5 14.51, p ,0.025).

The average area affected by Cliona on those shells thatwere bored (Fig 10B) was significantly greater after 6months at Panjang (average 11%) than at Cemara (aver-age 3.5%; t(4,10) 5 6.98, p , 0.001, data log transformed),but was not significantly different between the two sitesafter 1 year (Panjang, 11.1%; Cemara 18.3%; t(15,28)11.38,p.0.15). Because the average size of the bored area doesnot include unbored shells in the analysis, the average val-ue may remain unchanged or decrease as more shells be-come bored later in the study. At Panjang, no significantincrease in average area affected by Cliona was observedfrom 6 months to 1 year. At Cemara, a significant increaseoccurred from 6 months to 1 year (6 months, 3.5%; 12months, 18%, t(16,15) 5 4.17, p , 0.001, data log-trans-formed). The average area bored decreased from 1 to 2years, but this difference was not statistically significant(1 year 18.3%; 2 years 11.9%; t(15,27) 5 1.31, p.0.20).

Despite the low average Cliona cover, there was widevariance between shells, and Cliona occupied up to 60% ofthe area of individual shells (Fig. 10C). The rare shellswith a high degree of Cliona infestation indicate that ma-croborers are capable of colonizing and boring large partsof exposed shells within 1–2 years. Thus, differences in the


FIGURE 8—Encrustation and bioerosion of natural and fossil shells. Percentages of shell surfaces covered by animal encrusters, corallinealgae, and borings (primarily Cliona) are shown for 11 groups of shells (see Table 4 for descriptions of groups) from six environments:Semarang—clastic muds; Panjang—carbonate silt; Cemara—coral rubble; Batu Lawang—shallow carbonate sand; Lagun Marican, carbonatemud; and Taluk Awur (subfossil)—carbonate sand. Percent areal cover values are listed above each column. Cover was highest on hermittedshells from the productive clastic muds; living reclining Placuna from the same environment were less encrusted. Animal cover and boringintensity were high at Panjang, the eutrophic site, while algal cover predominated on shells from mesotrophic sites. Fossil shells had low ratesof encrustation and boring compared to shells collected on the seafloor.

FIGURE 9—Comparison of hermitted (A,B) and live collected (C,D) shells. Experimental Babylonia on the seafloor at the mesotrophic reef(Cemara, A) were encrusted by coralline algae and other organisms when occupied by hermit crabs; note Crepidula sp. near posterior edgeof aperture, and legs of crab in aperture. Turritella terebra dredged from siliciclastic muds at Semarang have few encrusters if alive, but havenumerous encrusting oysters and barnacles if occupied by hermit crabs (B).

frequency and extent of macroboring documented amongsites and treatments are not artifacts of the relatively briefduration of the experiments.

Interestingly, 7.1 % of the experimental Babyloniashells were drilled by an errant predator, probably a mur-icacean gastropod, suggesting mistaken predation as anadditional minor source of bioerosion (cf. Walker and Ya-mada, 1993).

Abundant microborings were present on elevated shellswhere encrustation was absent (Fig. 11). Microboringabundance, was not calculated, but SEM observationssuggest that microborings may contribute significantly tobioerosion on elevated shells. Shells on the sea-floor hadfewer microborings, particularly shells in eutrophic mudsin which microborings were rare (Fig. 11).

Natural shells were bored on average over 10–20% oftheir surface at the two experimental sites (Fig. 8), and

boring was significantly more abundant at eutrophic sitesthan mesotrophic sites (1-way ANOVA, F 5 7.29, p 50.05). The average values, however, include some relative-ly fresh shells with no borings and others that were rid-dled with borings. Shell cross sections revealed that up to70 percent of the shell volume may have been removed byCliona in otherwise intact shells. There was little-to-noshell boring at extremely muddy sites, such as siliciclasticmud at Semarang and carbonate mud at the mangrovesite.

Taphonomic Indicators

Weight Loss

Weight loss of shells on the sediment (Fig. 12) showedonly small differences between species and sites. The two


FIGURE 10—Bioerosion of shells in bags. (A) Percentage of shellswith bioeroding organisms (primarily Cliona), all taxa combined. (B)Average size of Cliona cover for shells with borings, all taxa combined.(C) Box plot showing medians, first and third quartiles, 95% confi-dence limits, and outliers of bioerosion through time, on all shell taxacombined. After 1 year 80–90% of the shells remain unbored, yetthose that were bored had on average .15% of shell surface boredby Cliona. Shells with up to 60% area bored indicate that macroborerscan quickly colonize large areas of shell. P6: Panjang, 6 months. C6:Cemara, 6 months. P12: Panjang, 12 months. C12: Cemara, 12months. C24: Cemara, 24 months.

FIGURE 11—Details of shell surfaces under SEM. After 1 year, Placunain bags on the seafloor at the eutrophic site (Panjang) are largely un-bored (A); elevated Placuna at Panjang (B) have extensive microbor-ings. Some A. inflata (C) on the seafloor at Panjang are slightly etchedand colonized by benthic foraminiferans (f). Placuna on the seafloor atthe mesotrophic site (Cemara) have limited microboring after 6 months(D). Scale bar is 50 mm in A,B and D; and 100 mm in C.

FIGURE 12—Weight loss of shells through time for all experimentalspecies, with 95% confidence intervals. Robust shells of A. inflata, A.granosa, and Paphia retained about 0.95 of the original weight up totwo years after deployment. Other species retained 0.85–0.90 of orig-inal weight probably as a result of chipping of fragile margins.

Anadara species and Paphia lost about 5% weight duringthe first one to two years at both sites. Striostrea and Pla-cuna with thin fragile margins and high organic contentslost 10–15% of weight during the study, significantly morethan the robust taxa (1-way ANOVA, F 5 18.6, p , 0.01).Results from the gastropod Babylonia were equivocal. Therapid initial decline in weight of Babylonia may reflect thedecay of soft parts which were difficult to fully extract pri-or to weighing; subsequent weight gain may reflect small

amounts of sediment trapped in the shell or internal en-crustation.

Fragmentation

Fragmentation during the study was limited mostly tomarginal chipping of species with fragile margins. In theshell bags, A. inflata, A. granosa, Babylonia, and Paphiasuffered little to no breakage, while Placuna and Strios-trea valves suffered minor chipping along their fragile


FIGURE 13—Average scorings for taphonomic attributes (see Table5) plotted through time for representative data sets; for complete datasee Appendix. (A) Fragmentation of Placuna, comparison betweensites and elevation; (B) Carbonate precipitation on three representa-tive shell-bag taxa from Cemara; no precipitation was observed onrack shells or at Panjang; (C) Color change for three taxa with shellcoloration: Babylonia, Striostrea, and Paphia in Cemara shell bags.Little fading of color was noted at Panjang; (D) Mineral staining onthree respresentative shell bag taxa at Jepara; no staining was ob-served at Cemara or on racks; (E) Periostracum of A. inflata; and (F)Ligament of A. inflata. Elevated shells degraded more rapidly thanbottom shells, but even 1–2 years after deployment, some shells re-tained periostracum and ligament, and suffered only light fading inelevated and sefloor treatments.

margins (Appendix). On the racks, A. inflata had minoredge chipping, but Placuna was eroded rapidly along theedges, until by after a year all that remained of most spec-imens was a small piece of shell, protected by the cable tie(Fig. 13A).

Precipitation and Dissolution

Carbonate precipitation, not directly attributable to epi-bionts (Fig. 13B), occurred on several shells at Cemara.The rough white precipitates are of unknown origin, butmay result from organic deposits of small unidentified en-crusters including coralline algae. No similar precipitationoccurred at Panjang. Evidence of dissolution was rare onall experimental shells (Appendix). Minor chalkiness andpitting was observed on the interiors of a few Striostreaand Paphia shells after one year in eutrophic muds; no pit-ting was noted at the mesotrophic site.

Color

There was little loss of color in the three pigmented spe-cies (Fig. 13C) during the study period. Tan mottled pat-terns on the snail Babylonia and the tan geometric patternon Paphia (batik clam is its local name) were mostly indis-tinguishable from live shells after one year. After 2 yearsmost shells were slightly faded, but retained some color.The purple coloration of Striostrea was degraded slightlyfaster, but remained visible in shell cross section. Panjangshells appeared to lose color more slowly than the Cemaraspecimens, but results were difficult to compare because ofmineral staining at Panjang.

Mineral Staining

Many experimental shells deployed in shell bags in theeutrophic muds (Panjang) underwent slight darkening af-ter 3 months, and pronounced mineral staining occurredfirst on about 20 to 30 % of the shells (depending on spe-cies) after one year (Fig. 13D). X-ray diffraction analysisshowed that these stains were Mg- and Fe- rich, and dom-inated by the iron oxy-hydroxides chamosite and goethite.There was no staining of shells on the seafloor at Cemara,or any elevated shells.

Periostracum

Four of the experimental species have periostraca asadults. Anadara inflata and A. granosa have hairy perios-traca, whereas Paphia and Babylonia have thin, hard,smooth periostraca. At the time of deployment, some Bab-ylonia shells were missing part or all of their periostraca;hence, these are not included in the analyses. Periostracaof A. inflata were the most susceptible to decompositionduring the study and began to erode between 3 (elevatedshells) and 6 months (bottom shells; Fig. 13E). However,after 1 year, almost all shells retained some periostraca(taphonomic score of 2), and approximately half retainedsome periostracum after two years on the sediment.

Ligament

Pieces of bivalve ligament remained on most shells forat least one year. The exception was elevated A. inflata atthe eutrophic site which completely lost the ligament by 6months (Fig. 13F). Ligament pieces remained on shells de-ployed on the seafloor through the final sampling intervalat the eutrophic (1 year) and mesotrophic (2 years) sites.Ligament data for A. granosa and Paphia (Appendix) aresimilar to those for A. inflata.

DISCUSSION

Limited Taphonomic Degradation

The results demonstrate that mollusc shells can persiston the seafloor with relatively little degradation for peri-ods of a year or more, even in tropical eutrophic environ-ments where biological activity is high. Among the shellsdeployed in bags on the sediment surface, there was nobreakage of shells, except for some minor marginal chip-ping in reclining Placuna and Striostrea, which may haveoccurred during deployment or retrieval. There was no ev-idence of edge rounding from abrasion. Anadara inflatashells elevated on racks had minor edge chipping. Theonly shells to have significant breakage were elevated Pla-cuna that had extensive erosion of their fragile margins,probably from grazing organisms.

All shells were disarticulated before deployment, butpieces of ligaments were retained on all shells for 6months and on most bottom shells for up to two years. Theendurance of ligaments on experimental shells suggeststhat natural shells may remain articulated for years afterdeath in areas of low turbulence and bioturbation. Like-wise, traces of periostraca lasted for at least a year on mostshells, including those elevated on racks. Periostraca didnot eliminate the settlement of encrusters (e.g., exterior


surfaces of A. inflata were encrusted heavily) and, thus,the eventual shedding of periostracum may alter the suc-cession of encrusters or separate encrusters from hostshells in the fossil record.

Color also was altered little over the course of the study.Among shells deployed on the seafloor at both sites, mostshells retrieved after one year were nearly indistinguish-able from live ones. By two years, most shells at Cemarawere somewhat faded, but clearly retained some of theiroriginal color. In instances where shells appeared white,the whiteness resulted primarily from encrusting coral-line algae. The original color patterns remained visible onunencrusted parts of the shells and in cross section.

Weight loss among shells deployed on the sediment sur-face was about 5% for the first two years in Anadara (bothspecies) and 10% for the other bivalves (Paphia, Placuna,Striostrea). These results are very similar to those foundin temperate shallow subtidal environments (Driscoll,1970). Weight loss in fragile species (e.g., Placuna, Strios-trea) probably results largely from marginal chipping andthe bacterial degradation of abundant organic matrix(Glover and Kidwell, 1993). In more robust species (e.g.,Anadara) weight loss is more difficult to explain. There islittle evidence of dissolution (under light microscope) andmicroboring (preliminary SEM observations); decay of or-ganic shell matrix and periostraca may be important fac-tors but require additional study.

Interspecies Differences

The experiments were designed to allow encrustationpatterns on shells of various shapes, textures, sizes, andstructures to be compared because marine larva select set-tlement sites based on these attributes. Statistical treat-ment of resulting patterns is difficult, however, becauseencrustation and boring rates of bag shells were very lowand there was wide variation between conspecific shells.The overall pattern that was observed was similar to thatdescribed by Best and Kidwell in Panama (2000b): be-tween species differences were small compared to inter-site differences.

Small size probably resulted in low encrustation in atleast one instance. Anadara inflata and A. granosa aresimilar in shape, texture, and mineralogy, and differmainly in that A. granosa is much smaller and had lowerrates of encrustation at both sites (Fig. 6). Among largehosts, other shell attributes may have been more impor-tant: A. inflata is heavily ribbed with a hairy periostrac-um, Babylonia is smooth, and Placuna is flat and primar-ily nacreous, yet all had high rates of encrustation.

Concave shell surfaces were encrusted more heavilythan convex surfaces initially; though convex cover in-creasingly became greater through time (Fig. 7). This pat-tern suggests that shells with limited exposure to encrust-ing larva would have most encrustation on concave surfac-es. For example, exhumed infaunal bivalve shells with lit-tle overall encrustation would be expected to have greatestencrustation on concave interior surfaces encrusted onlyafter the death and exhumation of the host. Greater en-crustation on convex surfaces, as is typical of many fossilshells (Lescinsky, 1995), would result primarily from epi-faunal shells that were encrusted during life. Shells thatwere exposed for several years after death might also have

greater convex encrustation, but would likely be dominat-ed by bioeroders.

The importance of shell composition to encrustation andbioerosion rates was difficult to test, in part, because ma-croborings occurred in such low rates. However, shell com-position did influence rates of fragmentation and weightloss. Shells with high organic content such Striostrea andPlacuna (Fig. 10) had high rates of shell weight loss, al-though this is complicated because these species also havethin margins that were chipped easily.

Although only observed inadvertently in this study, an-other factor affecting encrustation patterns is the habit ofa live host. Some experimental Babylonia became inhab-ited by hermit crabs; these shells were encrusted moreheavily than empty shells reclining in the mud (cf. Walk-er, 1989). Similarly, hermitted shells from the extremelysoupy muds of Semarang were encrusted heavily, whilelive hosts were unfouled. Host behavior also probably ac-counts for the high rate of encrustation of live Placuna inthe muds of Semarang as compared to other bivalve spe-cies with little encrustation. Placuna lives unattached andsedentary, but uses its foot to clear sediment from theshell surface (Young, 1980).

Experimental vs. Natural Shells

The high rates of encrustation and boring on naturalshells as compared to experimental shells suggests some-what different histories. Higher boring intensity of somenatural shells may reflect that these shells are older thanexperimental shells, and may have undergone several cy-cles of burial and exhumation (e.g., Meldahl et al., 1997).In contrast to the experimental shells with known histo-ries, natural shell were collected adjacent to reefs and mayhave been bored and encrusted on the reef prior to depo-sition in the softer muds at the reef margin. This is likelybecause only natural shells visible on the seafloor could becollected, and there were no visible shells in the muddy ar-eas distant from the reef. Therefore, natural shells mayrepresent an environment in which preservation of heavi-ly encrusted and bored shells is common—reef marginsbordered by muds.

Natural shells also contrast with the Holocene fossilshells, which were less bored and nearly devoid of encrus-ters. It may be that the natural shells collected from thesediment surface are atypical of the shells that actuallyenter the fossil record, which are dominantly shells sub-ject to rapid burial. Collections of natural shells usingdredges or suction, and therefore including shallowly bur-ied shells, may show much lower intensity of encrustationand bioerosion than observed in our natural shells fromthe sediment surface (Best and Kidwell, 2000a). The fos-sils represent a different environment than the eutrophicmuds to which they are currently adjacent. However, evenif the Holocene fossil shells are compared to natural shellsfrom a similar modern carbonate sand with similar taxa(our Batu site, Fig. 8), they still have low encrustation andbioerosion compared to the natural shells.

Effects of Productivity and Burial

Encrustation

Experimental results suggest that encrustation inten-sity and planktonic productivity are positively correlated


FIGURE 14—Effect of productivity on encrustation. Cover of encrus-ters is tied tightly to the available food source (productivity). For ce-ment settling plates, average percent encrustation is significantly pos-itively correlated with chlorophyll A concentration (r 5 0.95; Edingeret al., 1996). Experimental shells and natural shells were taken fromonly two sites with chlorophyll data; hence no correlation coefficientcan be calculated. Nonetheless, experimental elevated shells had sig-nificantly greater encrustation at the eutrophic study site than at themesotrophic study site. A similar, but much weaker, trend was evidentamong the natural shells from the two experimental sites.

on elevated substrates and for natural shells (Fig. 14). El-evated shells and cement tiles deployed at several sitesalong the same nutrient gradient (Edinger et al., 1996a)had higher rates of encrustation at eutrophic sites. Natu-ral shells exhibited a similar pattern to the experimentalshells, but the differences were less pronounced than onthe elevated substrates where sediment accumulationwasabsent.

Encruster type also was influenced by productivity. En-crusting organisms at the mesotrophic site were dominat-ed by autotrophs (e.g., coralline algae) or heterotrophswith low food requirements (e.g., bryozoans, rare discinis-cid brachiopods). In contrast, epibionts on shells in the eu-trophic environment included animals such as oysters,and barnacles that have relatively high biovolume, meta-bolic requirements, and growth rates.

Encrustation on shells in the bag experiments was notcorrelated with productivity, probably because the produc-tivity signal was overriden by the effects of sedimentation.Experimental bottom shells from mesotrophic sites weredusted only lightly with sediment and had greater encrus-tation than shells from the eutrophic sites which were bur-ied under 1–2 cm of sediment by 12 months. Best and Kid-well (2000a) found a similar pattern in Panama: little orno encrustation, bioerosion, abrasion, or dissolution oc-curred in nearshore siliciclastic facies, while higher ratesof these processes were documented in carbonate-rich fa-cies with longer exposure times of shells at the sedimentsurface.

Bioerosion

Bioerosion of shells, like encrustation, is controlled dom-inantly by planktonic productivity and burial. When bothproductivity and sedimentation are considered, bioerosionis highest in low sedimentation, high productivity set-

tings, such as eutrophic reefs in upwelling zones, and de-creases with increasing sedimentation (Edinger, 2001).

In this study, the low incidence of macroborings on bot-tom shells at both eutrophic and mesotrophic sites proba-bly results from both a time-lag in the establishment ofmacroborers and the protection of shells by rapid burial.Although most shells were unbored in both environments,patterns are evident among the minority of shells thatwere bored. First, at both sites, the frequency of shellsbored by Cliona increased over time, and increased fasterat the eutrophic site than at the mesotrophic site. The av-erage size of bored area on those shells with borings alsoincreased to about 10 to 15% of shell area at both sites.Shell area occupied by Cliona was highly variable, withmostly low cover values, but rare shells in each environ-ment had up to 70% of shell area bored (Fig. 10c). The highvariance for experimental shells (Fig. 10c) matches obser-vations from corals on the Great Barrier Reef and the JavaSea (Sammarco and Risk, 1990; Risk et al., 1995; Holmeset al., 2000).

The only statistically significant difference in boring be-tween sites was observed after six months, at which pointCliona colonies on shells at the eutrophic reef (Panjang)covered more shell area than Cliona colonies on shells atthe mesotrophic reef (Cemara). Similarly, sponge boreholesize was correlated positively with total bioerosion of mas-sive and branching corals, and with chlorophyll A concen-tration across the Great Barrier Reef (Edinger and Risk,1997).

Preliminary S.E.M. observations (Fig. 11) suggest thatshells on the sea floor, particularly those at the eutrophicsite, also had a low incidence of microborings during theinitial months of the study. Little microboring on the bot-tom shells probably results from low light levels and rapidburial. Most bottom shells at the eutrophic site were bur-ied 1–2 cm deep in mixed carbonate-siliciclastic mud after12 months, such that the frequency and intensity of shellbioerosion on these shells probably would not have contin-ued to increase through time. Microborings were abun-dant on elevated experimental shells.

Encrustation and Bioerosion as Indicators to AncientProductivity

Because the experimental results suggest that shell en-crustation and bioerosion are, in part, correlated with pro-ductivity, it is tempting to suggest that patterns of encrus-tation and boring in the fossil record may serve as a usefulindicator of past productivity (Lescinsky and Vermeij,1995). This suggestion appears to be borne out, as long asthe effect of burial is considered.

Elevated shells with no sedimentation (i.e., rack shells)had encrustation intensities that were proportional toplanktonic productivity (Fig. 14). Thus, in ancient envi-ronments with low sedimentation and sediment resuspen-sion (Fig. 15A,B), shell encrustation should provide an ac-curate indication of relative planktonic productivity.Shells from areas of low productivity (e.g., Cemara) willhave moderate encrustation (Fig. 15A) whereas shellsfrom productive sites (e.g., Panjang) will have higher en-crustation (Fig. 15B). Because low burial rates wouldcause skeletons to remain in the TAZ, external and inter-nal shell surfaces of epifaunal organisms will be encrust-


FIGURE 15—Interplay of planktonic productivity and burial in encrus-tation and bioerosion patterns.

ed, as will infaunal species that were exhumed to the sed-iment water interface.

An obvious complication of these predictions, however,is that high incidence of encrustation would be matched byhigh macroboring in areas of low sedimentation. Long ex-posure time might eventually allow complete destructionof shells prior to burial, except in environments of rapid,episodic burial (e.g., obrution deposits).

The types of encrusters that are present also provideclues to ancient productivity levels. Under low productivi-ty, such as at Cemara, encrusters had low biovolumes andcoralline algae were abundant. In low-light, outer shelf toslope environments with low productivity, algal encrus-ters are rare or absent, and encrustation may be restrictedto few small animal and protist encrusters (cf. Walker etal., 1998). Large biovolume animal encrusters are morecommon in productive waters.

Encrustation patterns may be most useful as indicatorsof ancient productivity in environments with soft bottomsand higher sedimentation (Fig. 15C, D). It is becoming in-creasingly clear from recent studies in Panama (Best andKidwell, 2000a), the Caribbean shelf (e.g., Parsons et al.,1999), and now the site at Panjang, that rapid burial is thenorm for shells on soft substrates. Therefore, shell encrus-tation would be limited primarily to the shells of live epi-faunal hosts that actively kept themselves clear of sedi-ment. This encrustation would likely be proportional toproductivity. Little post-mortem encrustation on shell in-teriors or exteriors and on infaunal shells would be expect-ed (Fig. 15D).

Few epifaunal organisms with skeletons inhabit softsubstrates today due, in part, to the rise of bioturbating or-ganisms (Thayer, 1979). Placuna is one of the few goodmodern analogues to the myriad of epifaunal brachiopodsand bivalves that inhabited Paleozoic seas. As a result,shell encrustation may be most useful as an indicator ofproductivity in Paleozoic soft bottom communities whenepifaunal host shells were commonplace.

Shell bioerosion is a more problematic indicator of an-

cient productivity. The results presented herein do showsome indications of increased macroboring in eutrophicwater, relative to the mesotrophic site. Natural shells atPanjang had greater boring cover than those at Cemara.Shells in the bag experiments had larger Cliona infesta-tions after 6 months at the eutrophic site suggesting amore rapid onset of boring. However, by 1 year, size of bor-ing was greater at the mesotrophic site suggesting thatburial rather than productivity may have become moreimportant.

A particular concern to studies of bioerosion in fossils isthat shells that are heavily bored may not enter the fossilrecord. Unburied shells in high productivity environmentsprobably experience very intense encrustation and bioe-rosion, to the point of complete shell destruction. The half-life of continuously unburied shells in high productivityenvironments has been estimated at 5 years (Edinger,2001).

Bioerosion from microborings and grazing is probablynot an accurate predictor of planktonic productivity. Mi-croborings are common in shells and corals in many shal-low tropical environments (e.g., Tudhope and Risk, 1985;Gunther, 1990; Radtke, 1993), but most microborers arecyanobacteria and green algae. Their distribution largelyis correlated with light and depth, and does not appear tovary directly with productivity (Chazottes, et al., 1995;Peyrot-Clausade et al., 1995). Fungi are also importantmicroborers, but may correlate with algal borers whichthey appear to consume (Henderson and Styan, 1982).

Experimental shells in this study suggest a possible in-verse relationship between productivity and microborings.Few microborings were observed on shells in the mud atPanjang, probably a result of partial burial and low lightlevels. At this site, light intensity at 6 m depth was re-duced to 1% of surface light intensity (Edinger et al.,2000a) and at 10 m where the experimental shell bagswere placed, conditions were quite dark, even during pe-riods of high visibility at the surface. Microborings werecommon on shells in the clear water Cemara site.

Similarly, grazing bioerosion probably does not corre-late with productivity in the fossil record. It is likely thatthe highest levels of grazing bioerosion on shells occur atmoderate levels of nutrients because highest productivityoften is achieved in turbid waters such that insufficientlight is available for endolithic algae and, hence, the graz-ing bioeroders that feed on them (Edinger, 2001). It is alsopossible that because shells are discontinuous ‘‘islands’’ ofsubstrate they are not as heavily grazed as corals. In anycase, microboring organisms and macroborings were thedominant forms of bioerosion that affected shells in Paleo-zoic shallow continental seas because external bioerodingorganisms (grazers) are mostly post-Paleozoic in origin(Vogel, 1993; Edinger, 2001).

While encrustation and bioerosion from macroborersare certainly informative general indicators of ancientproductivity, they are also highly sensitive to exposuretime at the sediment-water interface. Therefore, they areprobably most useful for understanding patterns on livehosts in soft bottom environments. For example, Walkerand Voigt (1994; Voigt and Walker, 1995) found that en-crustation on recent deep sea gastropod shells was higherin more productive waters. Many Paleozoic epeiric sea fa-cies with high encrustation (e.g., Kesling et al., 1980; Al-


exander and Scharpf, 1990; Lescinsky 1997; and manyothers) would probably also signal environments of highplanktonic productivity.

Rather than true bio-assays for ancient productivity,encrustation and bioerosion are relative indicators thatcan provide important clues of productivity in sedimenta-ry facies. Encrustation and bioerosion from macroborers,along with other macrofossil indicators of elevated foodlevels such as fast growth rates (Vermeij, 1980; Kirby,2001), large adult size (Vermeij, 1980; Naidu and Malm-gren, 1995), and low convexity of bivalved shells (Seed,1968; Vermeij 1990), can be used together with sedimentcharacteristics in fossiliferous deposits to help reconstructrelative patterns of ancient planktonic productivity.

SUMMARY

(1) There was little taphonomic degradation of shells in10 meters of water in mesotrophic and eutrophic reefs inup to two years of exposure. Fragmentation and color losswere low, whereas ligament and periostracum persistedthroughout the study.

(2) Rates of encrustation and bioerosion of experimentalshells reclining on the mud were most influenced by sedi-mentation and sediment resuspension. Shells on the sea-floor for up to two years had low rates of encrustation orbioerosion. Shells were bioeroded more intensely on theeutrophic reef than on the mesotrophic reef.

(3) Encrustation on elevated shells was high and posi-tively correlated with productivity. Encrusters on shells ineutrophic environments were dominated by large, highbiovolume animals, such as molluscs and barnacles, whileencrusters on shells in the offshore mesotrophic environ-ment were dominated by algae and low biovolume ani-mals, such as bryozoans. Encrustation on natural shellsalso correlated with productivity. The degree and type ofencrustation on fossil shells can serve as a useful indicatorof paleoproductivity. Frequency and intensity of bioero-sion may also help indicate paleoproductivity in facieswith equivalent shell exposure times.

ACKNOWLEDGMENTS

We are grateful to the villagers on whose reefs we con-ducted this study, and to field support from students andvolunteers including W. Atmoyo, D. Browne, G. Lemieux,D. Luxford, W. Mallchock, E.G. Setyadi, N. Waltho, andW. Widjatomoko. We also thank the staff of the Karimun-jawa National Marine Park for assistance in conductingfield research. D. Dingle assisted with sediment composi-tion analyses, and J.O. Ebbestad and D.J. Mercer assistedwith drafting maps. M. Best, P. Copper, J.O. Ebbestad, K.Parsons-Hurbbard, J. Rendell, L. Tapanila, and S. Walkerand several anonymous reviewers made helpful commentson the manuscript. Supported by the UNDIP-McMasterCoastal Ecodevelopment Project (CIDA Partnerships inCooperation and Development grant # 098/S47074-(0–99)), by a Geological Society of America student researchgrant to EE, and by an NSERC operating grant to MJR.EE thanks the Geology Department, St. Francis XavierUniversity, for computing and library support. Dedicatedto the memory of Rosa Halperin and Caleb Coughlin.

REFERENCES

AKPAN, E.B., and FARROW, G.E., 1985, Shell bioerosion in high-lati-tude low-energy environments: Firths of Clyde and Lorne, Scot-land: Marine Geology, v. 67, p. 139–150.

ALEXANDER, R.R., and SCHARPF, C.D., 1990, Epizoans on Late Ordo-vician brachiopods from southeastern Indiana: Historical Biology,v. 4, p. 179–202.

BAK, R.P.M., 1990, Patterns of echinoid bioerosion in two Pacific coralreef lagoons: Marine Ecology Progress Series, v. 66, p. 267–272.

BAK, R.P.M., 1994, Sea urchin bioerosion on coral reefs: Place in thecarbonate budget and relevant variables: Coral Reefs, v. 13, p. 99–103.

BELL, P.R.F., 1992, Eutrophication and coral reefs- some examples inthe Great Barrier Reef lagoon: Water Research, v. 26, p. 553–568.

BELLWOOD, D.R., 1995, Direct estimate of bioerosion by two parrot-fish species, Chlorurus gibbus and C. sordidus, on the Great Bar-rier Reef, Australia: Marine Biology, v. 121, p. 419–429.

BEST, M.M.R, and KIDWELL, S.M., 2000a, Bivalve taphonomy in trop-ical mixed siliciclastic-carbonate settings: I. Environmental vari-ation in shell condition: Paleobiology, v. 26, p. 80–102.

BEST, M.M.R, and KIDWELL, S.M., 2000b, Bivalve taphonomy in trop-ical mixed siliciclastic-carbonate settings: II. Effect of bivalve life-habits and shell types: Paleobiology, v. 26, p. 103–115.

BIRKELAND, C.E., 1977, The importance of biomass accumulation inearly successional stages of benthic communities to the survival ofcoral recruits: Proceedings, Third International Coral Reef Sym-posium, Miami, v. 1, p. 15–21.

BIRKELAND, C.E., 1989, Geographic comparisons of coral-reef process-es: Proceedings of the Sixth Coral Reef Symposium, v. 1, p. 211–220.

BROMLEY, R.G., and DE ALESSANDRO, A., 1990, Comparative analysisof bioerosion in deep and shallow water, Pliocene to Recent, Med-iterranean Sea: Ichnos, v. 1, p. 43–49.

BROMLEY, R.G., HANKEN, N.M., and ASGAARD, U., 1990, Shallow ma-rine bioerosion: Preliminary results of an experimental study:Bulletin of the Geological Society of Denmark, v. 38, p. 85–99.

BURNISON, B.K., 1980, Modified dimethyl sulfoxide extraction forchlorophyll analysis of phytoplankton: Canadian Journal of Fish-eries and Aquatic Sciences, v. 37, p. 729–733.

CHAZOTTES, V., LECAMPION-ALSUMARD, T., and PEYROT-CLAUSADE,M., 1995, Bioerosion rates on coral reefs: Interactions betweenmacroborers, microborers, and grazers (Moorea, French Polyne-sia): Palaeogeography, Palaeoclimatology, Palaeoecology, v. 113,p. 189–198.

CUTLER, A.H., 1995, Taphonomic implications of shell surface tex-tures in Bahia la Choya, northern Gulf of California: Palaeogeog-raphy, Palaeoclimatology, Palaeoecology, v. 114, p. 219–240.

DAVIES, D.J., POWELL, E.N., and STANTON, R.J.J., 1989, Relativerates of shell dissolution and net sediment accumulation—a com-mentary: Can shell beds form by the gradual accumulation of bio-genic debris on the sea floor?: Lethaia, v. 22, p. 207–212.

DAVIES, D.J., STAFF, G.M., CALLENDER, W.R., and POWELL, E.N.,1990, Description of a quantitative approach to taphonomy and ta-phofacies analysis: All dead things are not created equal: Paleon-tological Society Special Publication, No. 5, p. 328–350.

DE WILDE, P.A., KASTORO, W.J., BERGHUIS, W.W., ASWANDY, E.M.,AL-HAKIM, I., and KOK, A., 1989, Structure and energy demand ofthe benthic soft-bottom communities in the Java Sea and aroundthe islands of Madura and Bali, Indonesia: Netherlands JournalofSea Research, v. 23, p. 449–461.

DEWI, K.T., 1997, Ostracoda from the Java Sea, west of Bawean Is-land, Indonesia: Marine Geological Institute Special Publication,No. 4, 86p.

DRISCOLL, E.G., 1970, Selective bivalve shell destruction in marineenvironments, a field study: Journal of Paleontology, v. 40, p. 898–905.

EDINGER, E.N., 2001, Bioerosion: in Briggs, D.E.G., and Crowther,P.R., eds., Palaeobiology II: Blackwell, Oxford, p. 275–278.

EDINGER, E.N., and BROWNE, D.R., 2000, Continental Seas of West-ern Indonesia: in Sheppard, C.R.C., ed., Seas at the Millenium: AnEnvironmental Evaluation: Elsevier, Amsterdam, v. 2, p. 381–404.


EDINGER, E.N., and RISK, M.J., 1997, Sponge borehole size as a rela-tive measure of bioerosion and paleoproductivity: Lethaia, v. 29, p.275–286.

EDINGER, E.N., and RISK, M.J., 1998, Oceanography, sedimentology,and reef zonation in modern and ancient epeiric seas: The JavaSea as a modern analogue to the Devonian Appalachian Basin:Geological Society of America, Abstracts with Program, v. 30, p. A-39.

EDINGER, E.N., LUNDBERG, J., and RISK, M.J., 1996a, Holocene hyp-sithermal sea levels and local paleoceanography in the centralJava Sea from raised coral microatolls: Geological Society ofAmerica, Abstracts with Program, v. 28, p. A-303.

EDINGER, E.N., SETYADI, E.G., HANDOKO, P., BACHTIAR, T., and WID-JATMOKO, W., 1996b, Coral recruitment to artificial reef materialsin Indonesia: Abstracts, 8th International Coral Reef Symposium,Panama, p. 57.

EDINGER, E.N., JOMPA, J., LIMMON, G.V., WIDJATMOKO, W., and RISK,M.J., 1998, Reef degradation and coral biodiversity in Indonesia:Effects of land-based pollution, destructive fishing practices, andchanges over time: Marine Pollution Bulletin, v. 37, p. 617–630.

EDINGER, E.N., KOLASA, J., and RISK, M.J., 2000a, Biogeographicvar-iation in coral species diversity on coral reefs in three regions ofIndonesia: Diversity and Distributions, v. 6, p. 113–127.

EDINGER, E.N., LIMMON, G.V., JOMPA, J., WIDJATMOKO, W., HEIKOOP,J.M., and RISK, M.J., 2000b, Normal coral growth rates on dyingreefs: Are coral growth rates good indicators of reef health?: Ma-rine Pollution Bulletin, v. 40, p. 404–425.

EDINGER, E.N., LUNDBERG, J., and RISK, M.J., 2000c, Holocene fossilreef at Jepara, Central Java: A benchmark of pre-disturbancenearshore reef diversity and species composition?: 9th Internation-al Coral Reef Symposium, Bali, Abstracts, p. 49.

FLESSA, K.W., CUTLER, A.H., and MELDAHL, K.H., 1993, Time and ta-phonomy: Quantitative estimates of time-averaging and strati-graphic disorder in a shallow marine habitat: Paleobiology, v. 19,p. 266–286.

GLOVER, C.P., and KIDWELL, S.M., 1993, Influence of organic matrixon the post-mortem destruction of molluscan shells: Journal of Ge-ology, v. 101, p. 729–747.

GUNTHER, A., 1990, Distribution and bathymetric zonation of shell-boring endoliths in Recent reef and shelf environments: Cozumel,Yucatan (Mexico): Facies, v. 22, p. 233–262.

HANEBUTH, T., STATTEGGER, K., and GROOTES, P.M., 2000, Rapidflooding of the Sunda shelf: A late glacial sea-level record: Science,v. 288, p. 1033–1035.

HEIKOOP, J.M., RISK, M.J., LAZIER, A.V., EDINGER, E.N., JOMPA, J.,LIMMON, G.V., DUNN, J.J., BROWNE, D.R., and SCHWARCZ, H.P.,2000, Nitrogen-15 signals of anthropogenic nutrient loading incoral reefs: Marine Pollution Bulletin, v. 40, p. 628–636.

HENDERSON, C.M., and STYAN, W.B., 1982, Description and ecology ofRecent endolithic biota from the Gulf Islands and banks in theStrait of Juan de Fuca, British Columbia: Canadian Journal ofEarth Science, v. 19, p. 1382–1394.

HIGHSMITH, R.C., 1980, Geographic patterns of coral bioerosion: Aproductivity hypothesis: Journal of Experimental Marine Biologyand Ecology, v. 46, p. 177–196.

HOEKSTRA, P., 1993, Late Holocene development of a tide-inducedelongate delta, the Solo Delta, East Java: Sedimentary Geology, v.83, p. 211–233.

HOLMES, K.E., EDINGER, E.N., HARIYADI, LIMMON, G.V., and RISK,M.J., 2000, Bioerosion of live massive corals and branching coralrubble on Indonesian coral reefs: Marine Pollution Bulletin, v. 40,p. 606–617.

JOHNSON, M.E., 1987, Extent and bathymetry of North Americanplatform seas in the Early Silurian: Paleoceanography, v. 2, p.185–211.

KESLING, R.V., HOARE, R.D., and SPARKS, D.K., 1980, Epizoans of theMiddle Devonian brachiopod Paraspirifer bownockeri: Their rela-tionships to one another and to their host: Journal of Paleontology,v. 54, p. 1141–1154.

KIENE, W.E., and HUTCHINGS, P.A., 1992, Long-term bioerosion of ex-perimental coral substrates from Lizard Island, Great BarrierReef: Proceedings of the Seventh International Coral Reef Sym-posium, Guam, v. 1, p. 397–403.

KIENE, W.E., and HUTCHINGS, P.A., 1994, Bioerosion experiments atLizard Island, Great Barrier Reef: Coral Reefs, v. 13, p. 91–98.

KIRBY, M.X., 2001, Differences in growth rate and environment be-tween Tertiary and Quaternary Crassostrea oysters: Paleobiology,v. 27, p. 84–103.

KOWALEWSKI, M., GOODFRIEND, G.A., and FLESSA, K.W., 1998, High-resolution estimates of temporal mixing within shell beds: Theevils and virtues of time-averaging: Paleobiology, v. 24, p. 287–304.

LESCINSKY, H.L., 1993, Taphonomy and paleoecology of epibionts onthe scallops Chlamys hastata (Sowerby 1843) and Chlamys rubida(Hinds 1845): PALAIOS, v. 8, p. 267–277.

LESCINSKY, H.L., 1995, The life orientation of concavo-convex bra-chiopods: Overturning the paradigm: Paleobiology, v. 21, p. 520–551.

LESCINSKY, H.L., 1997, Epibiont communities: Recruitment and com-petition on North American Carboniferous brachiopods: Journalof Paleontology, v. 71, p. 34–52.

LESCINSKY, H.L., and VERMEIJ, G.J., 1995, Estimating ancient pro-ductivity: Shell-encrusting organisms as a paleo bio-assay: Geo-logical Society of America, Abstracts with Program, v. 27, p. A27.

MARSAGLIA, K.M., and KLEIN, G.D., 1983, The paleogeography of Pa-leozoic and Mesozoic storm depositional systems: Geology, v. 91, p.117–142.

MELDAHL, K.H., FLESSA, K.W., and CUTLER, A.H., 1997, Time-aver-aging and postmortem skeletal survival in benthic fossil assem-blages: Quantitative comparisons among Holocene environments:Paleobiology, v. 23, p. 207–229.

MILLIMAN, J.D., and MEADE, R.H., 1983, World-wide delivery of riversediment to the oceans: Journal of Geology, v. 91, p. 1–21.

MOKADY, O., LAZAR, B., and LOYA, Y., 1996, Echinoid bioerosion as amajor structuring force of Red Sea coral reefs: Biological Bulletin,v. 190, p. 367–372.

MORAN, P.J., and GRANT, T.R., 1989, The effects of industrial pollu-tion on the development and succession of marine fouling com-munities: Marine Ecology, v. 10, p. 231–246.

NAIDU, P.D., and MALMGREN, B.A., 1995, Monsoon upwelling effectson test size of some planktonic foramineral species from the OmanMargin, Arabian Sea: Paleoceanography, v. 10, p. 117–122.

NIXON, S.W., 1995, Coastal marine eutrophication: A definition, so-cial causes, and future concerns: Ophelia, v. 41, p. 199–219.

PANDOLFI, J.M., and GREENSTEIN, B.J., 1997, Taphonomic alterationof reef corals: Effects of reef environment and growth form. I: TheGreat Barrier Reef: PALAIOS, v. 12, p. 82–95.

PARI, N., PEYROT-CLAUSADE, M., LECAMPION-ALSUMARD, T., HUTCH-INGS, P.A., CHAZOOTES, V., GOLUBIC, S., LECAMPION, J., and FON-TAINE, M.F., 1998, Bioerosion of experimental substrates on highislands and atoll lagoons (French Polynesia) after two years expo-sure: Marine Ecology Progress Series, v. 166, p. 119–130.

PARSONS, K.M., POWELL, E.N., BRETT, C.E., WALKER, S.E., and CAL-LENDER, W.R., 1997, Shelf and slope experimental taphonomy ini-tiative (SSETI): Bahamas and Gulf of Mexico: Proceedings of the8th International Coral Reef Symposium 2, p. 1807–1812.

PARSONS-HUBBARD, K.M., CALLENDER, W.R., POWELL, E.N., BRETT,C.E., WALKER, S.E., RAYMOND, A.L., and STAFF, G.M., 1999, Ratesof burial and disturbance of experimentally-deployed molluscs:Implications for preservation potential: PALAIOS, v. 14, p. 337–351.

PARSONS, T.R., MAITA, Y., and LALLI, C.M., 1984, A Manual of Chem-ical and Biological Methods for Seawater Analysis: Pergamon, To-ronto, 171 p.

PETERSON, C.H., 1976, Relative abundances of living and dead mol-luscs in two California lagoons: Lethaia, v. 9, p. 958–965.

PEYROT-CLAUSADE, E.M., HUTCHINGS, P., and RICHARD, G., 1992,Temporal variations of macroborers in massive Porites lobata onMoorea, French Polynesia: Coral Reefs, v. 11, p. 161–166.

PEYROT-CLAUSADE, E.M., LECAMPION-ALSUMARD, T., HUTCHINGS, P.,LECAMPION, J., PAYRI, C., and FONTAINE, M., 1995, Initial bioero-sion and bioaccretion on experimental substrates in high islandand atoll lagoons (French Polynesia): Oceanologica Acta, v. 18, p.531–541.

POLUNIN, N.C.V., 1983, The marine resources of Indonesia: Ocean-ography and Marine Biology Annual Review, v. 21, p. 455–531.


APPENDIXExperimental Data

Treatment SiteMonths in

water# samples/

species A. granosa A. inflata Babylonia Paphia Placuna Striostrea

Total encrustation on internal surfaces

racksracksracksracksracks

PanjangPanjangPanjangCemaraCemara

36

1236

33333

0.330.980.940.230.76

0.440.680.920.330.51

bagsbagsbagsbagsbagsbags

PanjangPanjangPanjangCemaraCemaraCemara

36

126

1224

333332

0.010.000.020.030.110.06

0.030.000.030.030.110.20

0.020.050.030.080.160.16

0.020.050.030.060.150.16

0.020.040.040.080.160.24

0.030.030.040.080.230.12

Total encrustation on external surfaces



36

1236

33333

0.180.630.760.090.65

RADTKE, G., 1993, The distribution of microborings in molluscanshells from Recent reef environments at Lee Stocking Island, Ba-hamas: Facies, v. 29, p. 81–92.

RAGHUKUMAR, C., RAO, V.P., and IYER, S.D., 1989, Precipitation ofiron in windowpane oyster shells by marine shell-boring cyano-bacteria: Geomicrobiology Journal, v. 7, p. 235–244.

RASMUSSEN, K.A., and FRANKENBERG, E.W., 1990, Intertidal bioero-sion by the chiton Acanthopleura granulata; San Salvador, Baha-mas: Bulletin of Marine Science, v. 47, p. 680–695.

RISK, M.J., and MACGEACHY, J.K., 1978, Aspects of erosion of modernCaribbean reefs: Revista de Biologia Tropical, v. 2, p. 85–105.

RISK, M.J., SAMMARCO, P.W., and EDINGER, E.N., 1995, Bioerosion inAcropora across the continental shelf of the Great Barrier Reef:Coral Reefs, v. 14, p. 79–86.

ROBERTS, D., SOEMODIHARDJO, S., and KASTORO, W., 1982, Shallowwater marine molluscs of north-west Java: Lembaga OseanologiNasional, Jakarta, 143 p.

SAMMARCO, P.W., and RISK, M.J., 1990, Large-scale patterns in inter-nal bioerosion of Porites: Cross continental shelf trends on theGreat Barrier Reef: Marine Ecology Progress Series, v. 59, p. 145–156.

SEED, R., 1968, Factors influencing shell shape in the mussel Mytilusedulis: Journal of the Marine Biololgical Association of U.K., v. 48,p. 561–584.

SOKAL, R.R., and ROHLF, F.J., 1981, Introduction to Biostatistics:Freeman, New York, 363 p.

THAYER, C.W., 1979, Biological bulldozers and the evolution of ma-rine benthic communities: Science, v. 203, p. 458–460.

TJIA, H.D., 1980, The Sunda shelf, Southeast Asia: Zeitschrift Geo-morphologie, v. 24, p. 405–427.

TUDHOPE, A.W., and RISK, M.J., 1985, Rate of dissolution of carbonatesediments by microboring organisms, Davies Reef, Australia:Journal of Sedimentary Petrology, v. 55, p. 440–447.

VERMEIJ, G.J., 1980, Gastropod shell growth rate, allometry andadult size: in Rhoades, D.C., and Lutz, R.A., eds., Skeletal growthof aquatic organisms: Biological records of environmental change:Plenum Press, New York, p. 379–394.

VERMEIJ, G.J., 1990, Tropical Pacific pelecypods and productivity: Ahypothesis: Bulletin of Marine Science, v. 47, p. 62–67.

VOGEL, K., 1993, Bioeroders in fossil reefs: Facies, v. 28, p. 109–114.VOIGHT, J.R., and WALKER, S.E., 1995, Geographic variation of shell

bionts in the deep-sea snail, Gaza: Deep-Sea Research, v. 42, p.1261–1271.

WALKER, S.E., 1989, Hermit crabs as taphonomic agents: PALAIOS,v. 4, p. 439–452.

WALKER, S.E., and GOLDSTEIN, S.T., 1999, Experimental field ta-phonomy: Taphonomic tiering of molluscs and foraminifera aboveand below the sediment water interface: Palaeogeography, Pa-laeoclimatology, Palaeoecology, v. 149, p. 227–244.

WALKER, S.E., and VOIGHT, J.R., 1994, Paleoecologic and taphonomicpotential of deepsea gastropods: PALAIOS, v. 9, p. 48–59.

WALKER, S.E., and YAMADA, S.B., 1993, Implications for the gastro-pod fossil record of mistaken crab predation on empty molluscshells: Palaeontology, v. 36, p. 735–741.

WALKER, S.E., PARSONS-HUBBARD, K., POWELL, E.N., and BRETT,C.E., 1998, Bioerosion or bioaccumulation? Shelf-slope trends forepi-and endobionts on experimentally deployed gastropod shells:Historical Biology, v. 13, p. 61–72.

WYRTKI, K., 1961, Physical oceanography of Southeast Asian waters:Scientific results of marine investigations of the South China Seaand the Gulf of Thailand: NAGA Report, Scripps Institute ofOceanography, University of California, v. 2, 195 p.

YOUNG, A.L., 1980, Larval and postlarval development of the window-pane shell, Placuna placenta Linnaeus, (Bivalvia: Placunidae)with a discussion on its natural settlement: Veliger, v. 23, p. 141–147.

APPENDIX 1Experimental Data

Appendix lists the mean values for each class of experimental datarecorded. Number of shells available to calculate means are listed as‘‘N.’’ Total encrustation and boring are listed as proportions of the to-tal surface area; proportion of shells with borings refers to the propor-tion of shells that have at least one boring (Fig. 10A), average boringsize includes only shells with borings (Fig. 10B), weight loss is theproportion of the original weight remaining. Taphonomic attributes(fragmentation, precipitation, dissolution, color, mineral staining,periostracum, and ligament) are mean values according to the semi-quantitative framework in Table 5.

ACCEPTED OCTOBER 29, 2001


APPENDIXContinued


water# samples/




36

126

1224

303030303020

0.010.000.010.060.080.10

0.000.010.010.060.110.25

0.010.000.010.100.150.16

0.020.000.020.060.150.13

0.010.020.030.110.170.19

0.020.020.040.130.250.12

Total boring cover



36

1236

33333

00000

00000



36

126

1224

303030303020

0.000.000.000.000.020.04

0.000.000.030.010.030.05

0.000.010.000.000.000.03

0.000.010.000.000.010.01

0.000.010.050.000.020.01

0.000.010.080.000.010.02

Proportion of shells with borings



36

126

1224

303030303020

0.030.000.030.070.030.20

0.000.000.100.200.130.40

0.000.050.000.070.100.30

0.000.050.000.030.070.10

0.000.050.570.130.170.10

0.000.100.330.070.030.25

Average boring size



36

126

1224

303030303020

0.020.000.100.010.500.19

0.000.000.330.040.260.13

0.000.100.000.070.040.10

0.000.100.000.030.180.10

0.000.150.090.010.100.10

0.000.100.240.020.300.08

Weight loss

bagsbagsbagsbagsbags


36

126

12

33333

0.980.970.970.970.96

0.980.960.970.960.97

0.810.840.870.880.58

0.940.990.970.970.98

0.970.850.860.920.94

0.920.860.860.910.94

bags Cemara 24 2 0.96 0.95 0.92 0.91 0.9 0.9

Fragmentation



36

1236

33333

12.22.21.252

3.6744.524



36

126

1224

303030303020

111111

111111

111111

111111.2

1.522222

1.522222

Precipitation



36

1236

33333

11111

11111

11111

11111

11111

11111


APPENDIXContinued


water# samples/




36

126

1224

303030303020

111111

111111

1111.21.11.2

11111.21.2

1111.21.21.2

1111.11.451.4

Dissolution of interior surface



36

1236

33333

11111

11111

11111

11111

11111

11111


PanjangPanajangPanjangCemaraCemaraCemara

36

126

1224

303030303020

11111

11111

11111

111.2111.3

11111

111.1111

Color



36

126

1224

303030303020

111111.5

111112

111.011.11.561.7

Mineral staining



36

1236

33333

11111

11111

11111

11111

11111

11111



36

126

1224

303030303020

111.15111

111.27111

111.1111

111.23111

111.29111

111.18111

Periostracum



36

1236

33333

1.872.22.211.882.8



36

126

1224

303030303020

1.2221.882.52.5

1.32.162.161.82.52.7

111111

Ligament



36

1236

33333

23322



36

126

1224

303030303020

1.522222.5

1.52222.12.7

1.422222

Mollusc Shell Encrustation and Bioerosion Rates in a Modern ...

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