Coral reef development drives molluscan diversity increase...

� 2007 The Paleontological Society. All rights reserved. 0094-8373/07/3301-0002/$1.00

Paleobiology, 33(1), 2007, pp. 24–52

Coral reef development drives molluscan diversity increase atlocal and regional scales in the late Neogene and Quaternary ofthe southwestern Caribbean

Kenneth G. Johnson, Jonathan A. Todd, and Jeremy B. C. Jackson

Abstract.—The late Neogene was a time of major environmental change in Tropical America. Globalcooling and associated oceanographic reorganization and the onset and intensification of glaciationin the Northern Hemisphere during the past ten million years coincided with the uplift of the Cen-tral American isthmus and resulting changes in regional oceanographic conditions. Previous anal-yses of patterns of taxonomic turnover and the shifting abundances of major ecological guilds in-dicated that the regional shallow-water marine biota responded to these environmental changesthrough extinction and via a restructuring of local benthic food webs, but it is not clear whetherthis ecological response had an effect on the diversity of molluscan assemblages in the region.Changes in regional and local diversity are often used as proxies for similar ecological responseto environmental change in large-scale paleontological studies, but a clear relationship betweendiversity and ecological function has rarely been demonstrated in marine systems dominated bymollusks. To explore this relationship, we have compiled a data set of the stratigraphic and envi-ronmental distribution of genera of mollusks in large new collections of fossil specimens from thelate Neogene and Recent of the southwestern Caribbean. Analysis of a selection of ecological di-versity measures indicates that within shelf depths, assemblages from deeper water (51–200 m)were more diverse than shallow-water (�50 m) assemblages in the Pliocene. Lower diversity forshallow-water assemblages is caused by increased dominance of a few superabundant taxa in eachassemblage. This implies that studies of diversity of shelf benthos need to control for relatively finescaled environmental conditions if they are to avoid interpreting artifacts of uneven sampling astrue change of diversity. For shallow-water assemblages only, there was significant increase in localand regional diversity of bivalve assemblages after the late Pliocene. No parallel increase in gas-tropods could be detected, but this likely is because sample size was inadequate for documentingthe diversity of gastropod assemblages following a steep post-Pliocene decline of average gastro-pod abundance. Both the increasing bivalve diversity and the decrease in average abundance ofgastropod taxa correspond to an interval of increasing carbonate deposition and reef building inthe region, and are likely a result of increased fine-scale habitat heterogeneity controlled by thelocal distribution of carbonate buildups. Each of these results demonstrates that documenting theecological response of tropical marine ecosystems to regional environmental change requires alarge volume of fine-scaled samples with detailed paleoenvironmental control. Such data sets arerarely available from the fossil record.

Kenneth G. Johnson. Department of Palaeontology, The Natural History Museum, Cromwell Road, LondonSW7 5BD, United Kingdom. E-mail: [email protected]

Jonathan A. Todd. Department of Palaeontology, The Natural History Museum, Cromwell Road, London,SW7 5BD, United Kingdom. E-mail: [email protected]

Jeremy B. C. Jackson. Geosciences Research Division, Scripps Institution of Oceanography, University ofCalifornia, San Diego, La Jolla, California 92093-0244, and Smithsonian Tropical Research Institute, Box2072, Balboa, Republic of Panama. E-mail: [email protected]

Accepted: 25 September 2006

Introduction

Marine ecosystems of tropical America ex-perienced major environmental changes dur-ing the late Neogene that were associated withthe emergence of the Central American isth-mus (Coates et al. 1992; Collins et al. 1996b)and the onset and intensification of NorthernHemisphere glaciation (Raymo 1994). How-ever, we do not understand how biotic diver-sity responded to these changes in extrinsicfactors. One alternative is a simple relation-ship between the rate of diversity change and

the rate of environmental change, but diver-sity might also have remained stable, variedwithin limits around a dynamic equilibrium,or responded in a nonlinear fashion. Manynonlinear responses are possible. For example,ecological systems may be resistant to long-term environmental change until accumulatedchanges pass some threshold level, as has beenproposed for Caribbean coral reefs (Knowlton1992; Hughes 1994; Jackson 1994a; O’Dea et al.unpublished data). Even a lack of observablechange in diversity does not necessarily imply

25DIVERSITY OF NEOGENE MOLLUSCA FROM THE SW CARIBBEAN

a lack of change in taxonomic composition orecological function of communities; these at-tributes of communities are related in a com-plex manner (Tilman et al. 1998; Waide et al.1999; Mittelbach et al. 2001).

The late Neogene was a time of exception-ally strong global cooling and oceanographicchange (Zachos et al. 2001). Global coolingduring the past 10 Myr probably did not havea direct effect on tropical sea surface temper-atures until after 3 Ma. At this time, a gradu-ally shoaling oceanic thermocline passed athreshold at which cold waters could bebrought to the surface by winds in tropical up-welling zones. This shoaling of the thermo-cline in the Tropics triggered an amplificationof the obliquity component of Milankovitchcyclicity starting around 1.5 Ma, resulting inhigh-amplitude fluctuations in global ice vol-ume, sea level, and tropical sea surface tem-peratures characteristic of the middle and latePleistocene (Fedorov et al. 2006). The effects ofglobal cooling are confounded in the Carib-bean by the gradual rise of the Isthmus of Pan-ama with attendant changes in oceanographiccirculation and upwelling (Keigwin 1978; Hal-lock and Schlager 1986; Berger and Wefer1996; Haug and Tiedemann 1998; Allmon2001). These changes are recorded in the sed-imentary record of the isthmian region of thesouthwest Caribbean by an increase in depo-sition of calcium carbonate skeletal sedimentsand development of coral reef systems (O’Deaet al. unpublished data), and by decreasing in-fluence of seasonal upwelling of cold water asmeasured by annual range in water tempera-ture estimated from the size of bryozoan zo-oids (O’Dea et al. unpublished data) and var-iation of stable isotopes in mollusk shells (Col-lins et al. 1996a; Terranes et al. 1996). All ofthese long-term changes in the Caribbean mir-ror the differences today between the highlyproductive tropical eastern Pacific and the ol-igotrophic Caribbean (Birkeland 1987; Jacksonand D’Croz 1997). This modern contrast canbe used as an analogy for understanding pa-leoceanographic conditions and to help inter-pret Neogene faunal change in the Caribbean(Todd et al. 2002; Johnson and Perez 2006;O’Dea et al. unpublished data).

Previous work has documented regional

change in the late Neogene faunas of TropicalAmerica (Jackson et al. 1993; Jackson 1994b).These changes include a significant increase inthe rate of appearance and disappearance oftaxa within the southwestern Caribbean be-tween 3 and 1 Ma (Jackson and Johnson 2000),and major alteration of molluscan food websillustrated by a decrease in abundance ofpredatory gastropods and suspension-feedingbivalves (Todd et al. 2002). However, it is notclear what effect this late Neogene ecologicalshift would have had on taxonomic diversitywithin local communities. In this paper wedescribe in detail how the diversity of mollus-can genera in the southwest Caribbean re-sponded during the late Neogene environ-mental and biotic transition.

We can address this question rigorously forthe first time because of the quantity of bioticand stratigraphic information compiled overthe past 20 years by the Panama PaleontologyProject (Collins and Coates 1999b). These dataare based on large collections of shells from arange of environments within four deposi-tional basins along the Caribbean and ‘‘isth-mian’’ coasts of Panama and Costa Rica andinland in Darien Province, Panama (Fig. 1).The resulting compilation is internally consis-tent and can be analyzed within the context ofa state-of-the-art age model and a set of in-dependent proxies for paleoenvironment. Ourgeneral approach is to calculate a set of diver-sity estimates for local and regional assem-blages and to use these estimates to address aset of related questions including (1) Does thediversity of local assemblages of mollusksvary with water depth? (2) Are there signifi-cant correlations between the stratigraphicage and diversity of local assemblages withina limited range of water depths? (3) How isthe resulting pattern partitioned between gas-tropods and bivalves? (4) Does the pattern ob-served for local assemblages scale up to the re-gional level? and (5) How much information isrequired to produce an adequate descriptionof changes in paleobiodiversity of taxonomi-cally diverse groups within complex tropicalshallow-marine habitats?

Methods

Fossil Collections. Distributions of molluskswere obtained from samples collected by the

26 KENNETH G. JOHNSON ET AL.

FIGURE 1. A map of the southern Central America showing the geographical distribution of fossil collections fromthe Southern Limon, Bocas del Toro, Panama Canal, and Chucunaque-Tuira Basins. In contrast to the other threebasins that were sampled, the Chucunaque-Tuira Basin was not Caribbean but ‘‘isthmian’’ Pacific and was confluentwith the Panama Canal Basin during late Miocene and early Pliocene time (Coates et al. 2003). The distribution ofRecent dredge samples in Honduras (Cochinos Cays), Nicaragua (Miskitos Cays), and Kuna Yala (Panama, San BlasIslands) is also shown.

Panama Paleontology Project from the South-ern Limon Basin (Costa Rica), the Bocas delToro Basin (western Panama), Panama CanalBasin (Central Panama), and the Chucunaque-Tuira Basin (eastern Panama). Stratigraphicsections in these basins were described in detail(Coates et al. 1992; Coates 1999a,b; MacNeillet al. 2000; Coates et al. 2003, 2004a,b), and agemodels were developed using a combinationof biostratigraphic (Collins et al. 1996b; Aubryand Berggren 1999; Bybell 1999; Cotton 1999;Coates et al. 2004a), and paleomagnetic(McNeill et al. 2000) stratigraphy. Molluskswere recovered from a series of collectionstaken from the measured sections as de-scribed previously (Jackson et al. 1999). Thefossil component of the current data set differsfrom our previous paleontological compila-tions (Jackson et al. 1999; Todd et al. 2002) bythe inclusion of additional Miocene age col-lections from the Gatun Formation and equiv-alent-aged sediments of north-central Pana-ma, and extensive new Miocene material from

the Chucunaque-Tuira Basin of the DarienProvince of eastern Panama.

Recent Collections. Fossil occurrence rec-ords were supplemented with collections ofRecent mollusks obtained by dredging ofshallow shelf habitats in the southwestern Ca-ribbean. We analyzed collections from threesimilar-sized sampling regions, the CochinosArchipelago (Honduras), the Miskitos Cays(Nicaragua), and the San Blas Islands, KunaYala (Republic of Panama). Comparable Re-cent collections have been made from Bocasdel Toro but the mollusks from these have yetto be identified. Live and dead shells were col-lected from the dredge hauls, but the deadshells always constituted greater than 95% oftotal abundance. This time-averaging is likelyto be roughly similar to the time-averagingthat occurred during the preservation of thefossil assemblages. In the Bocas del Toro re-gion, Best and Kidwell (2000) have docu-mented the spatial fidelity of life and death as-semblages from samples recovered using col-


lecting gear and sieve mesh sizes identical toours, and Kidwell et al. (2005) documented ex-cellent preservation of shells in the siliciclas-tic-dominated settings but less-well preservedmaterial in carbonate-dominated substrata.For the current study, communities of mol-lusks were sampled from a range of habitatsand water depths including both carbonateand siliciclastic-dominated shelf settings.Hard-bottom habitats could not be sampledusing this dredging technique, but sampleswere made adjacent to carbonate platforms ineach of the basins. Collections were made be-tween 1995 and 1998 using surface dredges 70cm wide � 45–65 cm high with a 2.5 cm meshnet that were towed for distances of �50 toseveral hundred meters and always less than1 km (1–15 minutes tow-time). The area of sea-floor sampled is similar to the scale of a typ-ical area of rock outcrop from which fossil col-lections were assembled. The dredged sedi-ment was sieved through 8 mm and 2 mmmeshes then dried onboard ship. In the labo-ratory all identifiable mollusks (including bi-valve hinge fragments, gastropod apices, andfragmentary last whorls of gastropods) werepicked under a binocular microscope. Bivalveswere counted using the ‘maximum number ofindividuals’ approach advocated by Gilinskyand Bennington (1994) and protocols previ-ously established for the fossil collections(Jackson et al. 1999; Todd et al. 2002). Waterdepth, sediment characteristics, and the asso-ciated fauna were recorded and Van Veen grabsamples of sediment augmented the dredgedsubsamples for grain size, compositional, andfaunal analyses (O’Dea et al. unpublisheddata).

Identifications and Systematics. Protocols fortaxonomic identifications were developed toachieve high consistency and identifications ofeach taxon to the generic or subgeneric levelwere made according to our unified regionalsystematic framework for Neogene and Re-cent mollusks (Todd 2005a,b). Since our lastanalysis (Todd et al. 2002) the data have ben-efited from further improvements to this tax-onomic framework and by informal subgener-ic-level revisions of the regionally abundantand diverse genera of the neogastropod fam-ilies Turridae (sensu lato) and Cancellariidae,

as well as the smaller clade Coralliophilidae.Reference collections were compiled for bothfossil and Recent collections to illustrate thediagnostic characteristics of each genus orsubgenus; the fossil reference collection ishoused at the Naturhistorisches Museum Ba-sel, Switzerland, and the Recent is currentlyhoused at the Smithsonian Tropical ResearchInstitute, Ancon, Panama. Complete listings ofthe bivalve, gastropod, and scaphopod taxacan be found on the Neogene Marine Biota ofTropical America worldwide web site (Buddand Foster 2005) together with images of themajority of the bivalves and many of the gas-tropod taxa. At present the latter are repre-sented largely by taxa occurring within theGatun Formation of Miocene age.

Analyses have been made at generic/sub-generic level because within the collectionsthere are vast numbers of undescribed species,fossil and Recent, still requiring accurate de-limitation and documentation. The analyzeddata set includes all records that could beidentified to generic/subgeneric level withsome confidence and excludes those that couldbe identified only to a suprageneric level. Forthe present analysis we have tried to recog-nize all taxa believed to be distinct at the ge-neric or subgeneric level, whether formally de-scribed or not. For both recently revised andunrevised groups our taxonomic philosophyhas been to recognize as genera and subgen-era the smallest easily diagnosable and con-sistently recognizable, putative supraspecificclades, at least within the Neogene and Recentof the Neotropics. We have tried to ensure thatthe taxa we list and recognize are monophy-letic as far as is known with respect to othertaxa that either are in the collections or areknown to occur fossil or alive in the region.Through choosing morphologically tightlycircumscribed groups we have tried to bal-ance our desire for maximally useful genea-logical units—that are as close to species prox-ies as possible—with the pragmatic concernsof allowing reasonably rapid yet highly ac-curate identification (Todd 2001a). In analyz-ing the current data set our only departurefrom this protocol has been in cases where wehave had to lump the component subgenera ofa genus under a single analyzable name be-


TABLE 1. Numbers of genera/subgenera, occurrencerecords, and specimens of mollusks recovered from 489collections of fossil and Recent shells from the south-western Caribbean. Collections from faunules that wereinsufficiently sampled to obtain reliable diversity mea-sures were removed from the analysis, and are not tab-ulated here. Counts are provided for each class of mol-lusk and for all mollusks combined. An occurrence rec-ord is a record of a particular genus or subgenus froma particular sample. The number of samples in whicheach class occurred is also shown.

Class Taxa SamplesOccur-rences Specimens

Fossil � RecentBivalvia 261 462 7626 113,359Gastropoda 536 473 13,446 105,336Scaphopoda 16 279 503 5939TOTAL 813 489 21,575 224,634

Fossil onlyBivalvia 229 416 5424 82,770Gastropoda 494 427 11,882 98,349Scaphopoda 15 262 475 5755TOTAL 738 443 17,781 186,874

Recent onlyBivalvia 167 46 2202 30,589Gastropoda 215 46 1564 6987Scaphopoda 6 17 28 184TOTAL 388 46 3794 37,760

cause a significant proportion of the individ-uals assignable to that genus had not yet beenidentified consistently to subgeneric level. Incases in which a genus comprises multiplesubgenera and where more than 10% of the to-tal number of individuals identifiable to sub-generic level had been identified only to ge-neric level we merged the component subgen-era under the generic name and analyzed themore inclusive taxon. In these cases we alsomerged data from specimens assignable to ge-nus but not to subgenus because of incom-pleteness, juvenility, or wear. If less than 10%of the total number of individuals remainedunassigned to a subgenus pending furtherstudy, we discarded these records from theanalysis data set.

Data Sets and Analysis. The combined fossiland Recent data set for the southwestern Ca-ribbean includes 228,168 specimens of mol-lusks recovered from 519 collections compris-ing 814 genera and subgenera and includes22,136 occurrence (genus/subgenus per col-lection) records. This data set was convertedto an analyzable data set by removing assem-blages that were too small to provide usefuldiversity measures (see ‘‘Faunules and Strati-graphic Bins’’ below). Our analyzed fossil andRecent data set (Table 1) contains 813 generaand subgenera (just one fewer than the fulldata set), 489 collections (6% fewer), and a to-tal of 21,575 occurrence records (4% fewer).Within this compilation there are twice asmany gastropod genera and subgenera as bi-valves (536 gastropods, 261 bivalves) andnearly twice as many gastropod records as bi-valves (13,446 gastropods, 7626 bivalves), andscaphopods make up a small proportion ofthe total fauna (16 genera, 503 occurrence rec-ords, 5939 specimens). Other molluscan clas-ses are represented by very few specimens ofchitons and nautilids and were not analyzed.Previous fossil data sets included 1021 generaand subgenera (Jackson et al. 1999), decreas-ing to 782 (Todd et al. 2002) and now to 738in the current fossil data partition. The majorreduction in numbers between 1999 and 2002largely represents improved protocols forboth (1) applying open nomenclature in spec-imen identification in the case of taxonomic oridentification uncertainty (Bengtson 1988),

and (2) analyzing taxa in open nomenclature.In both the 2002 and current analyses we havebeen able to filter data of various degrees oftaxonomic uncertainty to achieve a balance be-tween improved taxonomic accuracy and po-tential loss of precision. The apparent reduc-tion in subgeneric diversity since 2002 is verylargely an artifact of ensuring identity of tax-onomic concepts between fossil and Recenttaxa through selective degradation of taxo-nomic data (see ‘‘Identifications and System-atics’’). Our analyzed fossil data partition in-cludes 80% more collections (443 versus 245)and almost 50% more specimens (186,874 ver-sus 127,000) than our 1999 compilation.

Paleodepth Estimates. Paleodepth data werecompiled by Jackson et al. (1999) from Collinset al. (1999), and are based on benthic fora-minifera with additional information from os-tracodes (Borne et al. 1999). Estimates fromthe Chucunaque-Tuira Basin were taken fromCoates et al. (2004a). The precision of paleo-depth assignments is variable, so we have an-alyzed depth within three broad depth classes(shallow: 0–50 m, intermediate: 51–100 m, and


deep: 101–500 m). The deepest assemblageswere recovered from mud facies interpretedas being deposited in depths of 200 m or more.These include the late Miocene assemblagesfrom the Nancy Point Formation of the Valien-te Peninsula, Bocas del Toro Basin, and the Us-cari Formation of Rio Sand Box, Southern Li-mon Basin (Jackson et al. 1999; Coates et al.2003). The Recent assemblages were analyzedwithin the same depth classes. The deepestRecent sample was recovered from a waterdepth of 80 m in the Cochinos Cays, Hondu-ras.

Faunules and Stratigraphic Bins. We com-pared diversity over time and depth at twosampling scales: faunules and stratigraphicbins. Although collections-level data wereavailable, many collections were too small toprovide adequate estimates of taxonomic di-versity. At this small spatial scale, diversitymeasures may vary on complex patterns be-cause they are strongly influenced by both thehigh local variability in species richness typi-cal of marine benthic invertebrate communi-ties (Ellingsen 2001; Shin and Ellingsen 2004)and local geological vagaries of taphonomy,diagenesis, and weathering. Instead, we usedfaunules as the primary unit of analysis. Faun-ules are assemblages recovered from a set ofcollections from a limited stratigraphic inter-val and geographic distribution (Jackson et al.1999). Fossil faunules were defined by the age,location, and general lithology of a particularstratigraphic unit. Collections included ineach faunule were recovered within 20 m ofstratigraphic section and generally along lessthan 1 km of outcrop in maximum dimension,though exceptionally up to 3.1 km in linear ex-tent where faunas or exposures were limited(Shark Hole Point and Rio Sand Box faunules).Substrate type is an important factor control-ling the membership of faunules, and there-fore faunules include collections taken from asingle lithostratigraphic formation. The faun-ules defined by Jackson et al. (1999) were com-bined with newly defined faunules from riverexposures in the Chucunaque-Tuira Basin(Coates et al. 2004a,b) and coastal exposurescurrently referred to the Gatun Formation innorth central Panama. Faunules for the Recentassemblages were defined herein by grouping

dredge samples by geography and waterdepth. Collections constituting Recent faun-ules have dredge start points sited within a to-tal of 3.1 km distance of each other, exception-ally 3.7 km (San Blas�1�1 faunule) and, as forthe fossil faunules, frequently within 1 km. Forfossil units, faunules include only collectionstaken from a single formation, so the substratetypes are restricted to those available within aformation. Recent collections were obtainedby dredging, so some mixing of local sub-strate type was unavoidable. For practical rea-sons, sites characterized by soft mud or sandsubstrata were preferred over reef or otherhard-bottomed substrata that would havedamaged the sampling equipment.

A total of 94 faunules were defined, includ-ing 60 fossil faunules and 34 Recent faunules.However, faunules that contained fewer than100 specimens or ten taxa were removed fromthe analysis because these sample sizes wereinadequate to provide usable estimates of tax-onomic diversity. This resulted in the removalof only 16 faunules, 12 fossil and 4 Recent,comprising 26 collections and 612 specimens.Age and depth assignments of each faunulewere based on the total range in age anddepth of all collections included in the faunule.A list of faunules, estimated ages, and thenumber of collections, specimens, and taxa areincluded as an appendix available online atdx.doi.org/10.1666/06022.s1, and the fullanalysis data set is available at the NMITA da-tabase (Budd et al. 1996–2006).

The data were also analyzed within a set ofstratigraphic bins. Selection of bins was basedon the stratigraphic distribution of collections(Fig. 2) in order to establish approximatelyuniform numbers of collections per strati-graphic bin. We also considered the relativestratigraphic resolution of collections in orderto avoid assigning collections to narrow timebins in cases of imprecise age estimates. Thecompromise solution was a set of bins of un-equal duration with boundaries at 13, 11, 8.3,5.4, 3.7, 3.4, 2.2, 1 Ma, and the Recent. The firstthree bins correspond to the middle Miocene,the early late Miocene, and the late late Mio-cene. The bin from 5.4 to 3.7 Ma includes theearly Pliocene samples, and the narrow Plio-cene bin from 3.7 to 3.4 Ma corresponds to the


FIGURE 2. Range chart showing the stratigraphic rang-es assigned to each faunule included in the analysis. The30 Recent faunules are illustrated with exaggeratedranges for improved visibility. The dashed horizontallines indicate the nine stratigraphic subintervals consid-ered in the text.

lower part of calcareous nannoplankton zoneNN16 (Berggren et al. 1995). A number of col-lections that were recovered from sectionswithin the Cayo Agua and Escudo de Vera-guas Formations (Bocas del Toro Basin) andthe Rio Banano Formation (Southern LimonBasin) were correlated with that biozone (Au-bry and Berggren 1999). Collections from thelate Pliocene interval (3.4 to 2.2 Ma) includerich assemblages from the Bocas del Toro andSouthern Limon Basins. The interval between2.2 and 1.0 Ma includes the period character-ized by increased taxonomic turnover of gen-era within the southwestern Caribbean (Jack-son 1994b; Jackson and Johnson 2000), and in-cludes a set of collections from the Moin For-mation of the Southern Limon Basin and SwanCay from the Bocas del Toro Basin. To com-bine collections into faunules and stratigraph-ic bins, we merged taxonomic lists by addingnumbers of specimens for shared taxa in eachfaunule. Therefore, diversity estimates for thefaunules and the stratigraphic intervals do notrepresent averages of diversity estimated forcollections within each sampling unit. Esti-mates of generic diversity for the stratigraphicbins were calculated using only taxa that ac-tually were recovered from a particular inter-val.

Collections were not distributed uniformlywith respect to time or paleoenvironment (Ta-ble 2, Fig. 2). The youngest marine depositspreserved in the four basins generally increase

in age to the east, so although Miocene, Plio-cene, and Plio-Pleistocene collections were re-covered from the more westerly Bocas delToro and Southern Limon Basins, the collec-tions from the Canal and Chucunaque-TuiraBasins of central and eastern Panama are ex-clusively Miocene in age. The distribution ofpaleodepths is also uneven, collections de-rived from the Miocene of the westerly Bocasdel Toro and Southern Limon Basins are ob-tained from sediments deposited in deeperwater, the Canal Basin contains shallow (�50m) and intermediate-depth deposits (51–100m), and the collections from the eastern basinswere obtained primarily from shallow-waterfacies (�50 m). Pliocene collections from Bo-cas del Toro Basin were recovered from sedi-ments deposited in shallow (�50 m), inter-mediate (51–100 m), and deep-water (101–500m) settings. A broad selection of environ-ments were also sampled from the Plio-Pleis-tocene sediments of the Southern Limon Ba-sin, but over two-thirds of the collections wereobtained from facies with paleodepth be-tween 51 and 100 m. The Recent samples weredredged from shallow (�50 m) and interme-diate (51–100 m) depths off the Cochinos Cays(Honduras) and San Blas (Kuna Yala, Pana-ma), but the Miskitos Cays (Nicaragua) sam-ples are solely from shallow water (�50 m).Such unevenness in sampled bathymetricranges precludes analysis of geographic pat-terns of changes in diversity among basins.Nevertheless, the distribution of samples andenvironments is adequate to examine withconsiderable confidence changes in diversityover time in shallow water and among depthswithin the Pliocene.

Diversity Measures. We used taxonomicrichness (G), Fisher’s alpha (�), and Shannon’sH to describe the generic diversity of collec-tions, faunules and stratigraphic bins. Magur-ran (2004) distinguished between three gen-eral classes of diversity indices: taxon richnessindices, parameters from taxon abundancemodels, and indices that incorporate propor-tional abundances of taxa. Each approach hasstrengths and weaknesses, and here we haveselected one widely used index from eachclass. Taxonomic richness (G) is the number ofgenera or subgenera in each assemblage. In


TABLE 2. Distribution of samples of fossil and Recent assemblages of mollusks from the southwest Caribbean.Numbers of samples from each basin are shown. Beta diversity (�) calculated using samples within each basin werecalculated following the methods of Schluter and Ricklefs(1993).

Fossil

Age (Ma) DepthBocas del

ToroPanamaCanal

Chucu-naque Limon

NW coastPanama Total � 1/�

1/(��N)

2.2–1 �50 m 1 1 — — —51–100 m 1 2 3 0.549 1.82 0.61

101–500 m 1 1 2 0.792 1.26 0.633.4–2.2 �50 m 1 3 4 0.677 1.48 0.37

51–100 m 1 1 — — —101–500 m 1 1 — — —

3.7–3.4 �50 m 1 3 4 0.579 1.73 0.4351–100 m 3 1 4 0.559 1.79 0.45

101–500 m 2 2 0.671 1.49 0.755.4–3.7 �50 m 3 1 4 0.526 1.90 0.48

51–100 m 1 1 — — —101–500 m 2 2 0.723 1.38 0.69

8.3–5.4 �50 m 5 5 0.442 2.26 0.4551–100 m 2 1 3 0.744 1.34 0.45

101–500 m 2 1 3 0.682 1.47 0.4911–8.3 �50 m 3 1 2 6 0.424 2.36 0.39

�11 �50 m 1 1 2 0.802 1.25 0.62TOTAL 21 5 7 13 2 48

Recent

Region Depth

Cochinos Cays �50 m 7 0.308 3.25 0.4651–101 m 4 0.491 2.04 0.51

Miskitos Cays �50 m 9 0.304 3.29 0.37San Blas �50 m 7 0.363 2.75 0.39

51–101 m 3 0.633 1.58 0.53TOTAL 30

much ecological notation, S is used to signifytaxonomic richness, but here we use the sym-bol G to emphasize that we are not working atthe species level. Richness is easy to interpretas a measure of diversity, but it is highly sen-sitive to sample size. The majority of taxa arepresent in low abundance in all samplingunits, so it is difficult to determine whetherdifferences in richness among sampling unitsare an artifact.

Because it is known that raw taxonomicrichness correlates strongly with sample size,we used a subsampling approach to comparerichness among faunules and stratigraphic in-tervals. This procedure is similar to the ana-lytical rarefaction method (Tipper 1979) inthat diversity is estimated from a uniformnumber of specimens in each faunule. In ourcase, diversity measures are calculated as me-dians of the distribution of richness estimatedfrom a set of reduced assemblages, whichwere produced by random selection of a fixed

number of specimens from each total faunuleassemblage. The approach is similar to thesubsampling methods of Alroy et al. (2001),except that our method explicitly includes tax-on abundance because we are subsampling ac-tual specimen occurrence records rather thanoccurrences records from lists of taxa. Selec-tion of sampling size used to normalize totalfaunule abundance requires a compromise be-tween interpreting low abundance as eitherreal or sampling artifact in the absence of anobjective measure of true sampling effort. Di-versity was estimated from faunules reducedto 250, 500, 1000, and 2000 specimens, and thepatterns obtained were similar, so results areonly shown for faunules rarefied to 250 spec-imens (G250). Therefore, we have a total of fourmeasures of diversity that can be comparedon several spatial scales.

Fisher’s alpha (�) is one of the many diver-sity indices derived from fitting the observeddata to a theoretical abundance distribution


(Hayek and Buzas 1997). In this case, is oneparameter of a log-series distribution estimat-ed using the numbers of specimens (N) andnumber of genera (G) recovered from a sam-pling unit. If the taxon abundance distributionfollows a log-series distribution then � will beindependent of sample size (N). A simple in-terpretation of � is that it approximates thenumber of taxa represented by a single spec-imen in each assemblage. As an index of di-versity, � is more dominated by richness thanby taxonomic evenness within an assemblage.For this study, � was estimated using the op-timization method outlined by Hayek andBuzas (1997). The variance of � for each sam-pling unit was estimated using Fisher’s for-mula reproduced by Hayek and Buzas (1997:equation 9.17).

The relative abundance of taxa within sam-pling units is not used to estimate G or �.Shannon’s index (H) is one of the most com-monly used diversity indices that does incor-porate data on proportional abundance. How-ever, H is moderately sensitive to sample size,because it is sensitive to the number and abun-dance of rare taxa (Magurran 2004). The var-iance of H was estimated using the formuladerived by Hayek and Buzas (1997, equation13.8). Unlike �, H is a nonparametric measureof diversity because it does not require as-sumptions regarding the underlying distri-bution of abundances within each assemblage.Although the value of H is determined by boththe number of taxa and the proportion of eachtaxon in an assemblage, it is more stronglyweighted by richness than by the relativedominance of abundant and rare taxa. Thestatistical programming language R was usedfor all analyses (R Development Core Team2005).

Beta Diversity. Beta diversity within eachstratigraphic/depth bin was calculated as theinverse of the average number of faunulesfrom which each taxon was recovered in eachbin (Schluter and Ricklefs 1993) (Table 2). Forthis calculation all sites were used within eachstratigraphic/depth bin. Beta diversity is ameasure of the contribution of meso-scalepatchiness to regional diversity within eachinterval so that bins composed of assemblagesthat are more variable in composition will

have higher beta diversity indices than binscharacterized by local assemblages with moreuniform composition. We normalized the betavalue for sampling bias by considering the av-erage proportion of faunules from which eachtaxon has been recovered in each time interval(1/(�·N)) (Schluter and Ricklefs 1993).

Ecological Groups. Previous macroecologi-cal analysis of southwest Caribbean mollus-can faunas has uncovered changes in life hab-its at a coarse temporal resolution, indicatingmajor changes in food webs that are consistentwith a decline in regional productivity and in-crease in reefal habitats (Todd et al. 2002).Here we use the same autecological data set(Todd 2001b) at a more refined temporal scaleto examine whether any changes in diversityare associated with increases in hard-sub-strate-dwelling mollusks indicative of reefalenvironments. We completed analyses of bothabundance and generic/subgeneric diversityas proportions of the total fauna recordedwithin each stratigraphic bin. Molluscan lifehabits were inferred from shell morphologyand by analogy with living representatives ofgenera, and include the relationship to thesubstrate, mobility, and shell attachment. Bi-valves considered characteristic of the hardsubstrata common in coral reef habitats in-clude those possessing any of the followinglife habits: immobility, cementation, boring, ornestling (categories IM, CE, WN, and WB ofTodd 2001b, respectively).

Results

Local Diversity and Abundance. The numberof specimens recovered from each faunulevaries over two orders of magnitude, from 100to over 17,000 specimens (Fig. 3A). Conspic-uously specimen-rich fossil faunules compris-ing over 10,000 specimens include Bomba,Ground Creek, Isla Payardi, Martin LutherKing, Mattress Factory, and Quitaria (Appen-dix). All of these faunules comprise assem-blages deposited in depths of less than 50 mand were obtained from Miocene and Pliocenesediments. These high apparent abundancesare due to varying combinations of high sam-pling intensity and original shell density. Forexample, Bomba, Isla Payardi, Martin LutherKing, and Quitaria include sites that have


FIGURE 3. The number of specimens and generic diversity estimated for faunules, with 95% confidence intervalsshown for H and �. A, The number of specimens recovered from each faunule (N). B, The total number of generaand subgenera found within each faunule (G). C, Median number of genera and subgenera recorded in each faunuleafter repeated subsampling of 250 specimens at random (G250). D, Fisher’s �. D, Shannon’s H.

been sampled repeatedly (Appendix). In con-trast, the very shelly strata at Ground Creekand Mattress Factory probably represent sea-grass assemblages as shown by their abun-dance of numerous chionine bivalves, Bulla,

and minute detritivorous gastropods. The IslaPayardi faunule also includes specimen-rich,turritellid-dominated assemblages that typi-cally develop in habitats characterized by softsediment and high planktonic productivity


(Allmon 1988). Among the Recent faunules,Nicaragua faunules 3 and 10 and San Blasfaunules 8 and 9 all contain more than 3000specimens each. These faunules are similar inbeing bivalve-dominated with superabundanttaxa characteristic of shifting sands (Tucetona,Crassinella), and taxa tolerant of dysoxic sedi-ments (abundant lucinids, protobranchs andcorbulids), together with common epifaunalbivalves (Arca, chamids) and detritivorousgastropods (Cerithium, Modulus) (e.g., Bitter-Soto 1999; references in Todd 2001b). Theseassemblages each signal strongly heteroge-neous substrata that typify reef-associated fa-cies; these include detritus-rich seagrassmeadows, less vegetated sands, and patchreefs and reef rubble associated with theslopes of reef patches.

Local richness of genera (G) varies from 13to 260 in total assemblages with a median of129 (Fig. 3B). After rarefaction to 250 speci-mens (Fig. 3C), this median decreases to 63because of the removal of large numbers ofgenera represented by only a few specimens.As measured by G250, the richest faunules wereobtained either from fossil assemblages de-posited in intermediate or deep water or fromshallow-water assemblages from the Recent.Rich fossil faunules are derived from Pliocenesediments deposited in the Bocas del Toro andLimon Basins, including Fish Hole, north-cen-tral Escudo de Veraguas, northeast Escudo deVeraguas, and Lower Lomas del Mar East(non-reef) faunule. The fossil faunule depos-ited in shallow water with the highest richnessis Isla Solarte, from the Bocas del Toro Basin.However this faunule ranks fourteenth in rich-ness and is less rich than each of seven fossilfaunules deposited in deep or intermediate-depth water, six Recent faunules deposited inshallow water, and one Recent faunule depos-ited in intermediate-depth water. Recent faun-ules with G250 greater than 70 comprise shal-low and intermediate-depth water assemblag-es from Honduras (faunules 1, 3, and 7), Nic-aragua (faunule 7), and San Blas (faunules 1and 10) (see Appendix). All of these Recentfaunules consist of heterogeneous assemblag-es typifying seagrass facies and reef-associat-ed lagoons. Among the indicators are abun-dant deposit feeders from organic-rich sedi-

ments (protobranchs, tellinids), infaunal sus-pension feeders in clean sands in seagrassfacies (for example, Chione and Tucetona), sea-grass-dwelling epifauna, including detriti-vores (for example Cerithium and Modulus)and suspension feeders (Arcopsis, other ar-coids), as well as sand-patch dwelling snailsand bivalves (for example, Strombus and Ar-gopecten) (Jackson 1973; Bitter-Soto 1999; ref-erences in Todd 2001b).

Fisher’s � varies from 10 to 56 (Appendix).Particularly diverse fossil faunules (� greaterthan 40) include Cayo Agua (Punta PiedraRoja West), Cayo Agua (Punta Tiburon toPunta Piedra Roja), Fish Hole, Lower Lomasdel Mar East (non-reef) and Upper Lomas delMar East Reef tract, all obtained from Plioceneto Pleistocene reefal and seagrass habitats(Jackson et al. 1999; see below). Notably, theCayo Agua faunules contain many genus-leveltaxa typical of seagrass environments of cen-tral Florida today (Hill 2002). Deeper water,exceptionally well preserved, mud-dwellingfaunas from the middle to late Pliocene Es-cudo de Veraguas Formation (north-central,northeast, and southeast Escudo de Veraguasfaunules) are also of noticeably high diversity.Recent faunules with � greater than 40 includeSan Blas faunules 1, 8, and 9. San Blas 1 faun-ule comprises taxa strongly indicating thepresence of seagrass environments (notedabove) and rarer taxa characteristic of reefrubble, such as chamid bivalves.

Shannon’s H varies between 1.6 and 4.3, butexceptionally can be as low as 1.5. As for Fish-er’s �, diverse fossil faunules (H greater than4) include north-central and southeast Escudode Veraguas, Fish Hole, Cayo Agua (Punta Ti-buron to Punta Piedra Roja), and Lower Lo-mas del Mar East (non-reef). All except theCayo Agua faunule were deposited at waterdepths greater than 50 m in mud (Escudo deVeraguas) or clearly seagrass or fore-reef hab-itats (Fish Hole, Lower Lomas del Mar East[non-reef]). For example, the Cayo Agua faun-ule contains abundant Olivella, Tucetona, cor-bulids, Crassinella, and other taxa typical ofseagrass and associated habitats at the presentday (Hill 2002). The sole Recent faunule show-ing Shannon’s H greater than 4 is Honduras�1.This faunule includes abundant shells of Chi-


FIGURE 4. Comparison of abundance and generic diversity measures for faunules. Pairwise plots of numbers ofspecimens (N), total and rarefied numbers of genera and subgenera (G and G250), Fisher’s �, and Shannon’s H areshown. Kendall’s correlations are shown in the lower right corner of each plot. The asterisks indicate the significancelevel of tests of the null hypothesis of each correlation being equal to zero. A single asterisk indicates that the nullhypothesis was rejected at a level of 0.05, and double asterisks indicate that the null hypothesis was rejected at asignificance level of 0.01.

one, corbulids, Chama, Arca, Bulla, and othertaxa consistent with seagrass environments.The abundance of Smaragdia, an obligate sea-grass-dwelling neritid snail, confirms this in-terpretation. Previous studies of the diversityof mollusk assemblages within a range of col-lection to basinal scales were performed dur-ing taphonomic studies of reef and reef-asso-ciated deposits of the late Pleistocene of theBahamas (Gardiner 2001) and the Recent ofPuerto Rico (Parsons-Hubbard 2005). Thesestudies appear to show a pattern similar tothat observed in the southwestern Caribbean.In each study generic and/or species richnessand Shannon’s H are highest in reef and sea-grass environments when compared withneighboring unvegetated shallow sands andmuds.

Comparison of Diversity Measures. There issignificant correlation between unrarefied Gand �, and the number of specimens in each

faunule (N), but not between rarefied G (G250)or H and N (Fig. 4). This indicates that rare-faction is reducing sampling bias as hoped.The correlation of � with N indicates that thedistribution of taxon abundance in these mol-luscan faunas does not exactly correspond toa log-series distribution (Buzas and Hayek2005). The shape of a log-series distribution isspecified by two parameters, � and x, andgoodness of fit between the observed data anda log-series distribution can be approximatedby the value for x. Values of x greater than 0.95are considered to represent exceptional fit(Hayek and Buzas 1997). One-third (n � 30)of the Recent faunules are characterized byvalues of x lower than 0.95, and x is also lessthan 0.95 for 12.5% (n � 48) of the fossil faun-ules (Appendix). This lack of fit may be ex-plained by our having sampled from a singleabundance distribution that does not follow alog-series distribution, or having sampled


TABLE 3. Mean number of specimens and diversity of Pliocene faunules classified by inferred water depth. Stan-dard errors are shown in parentheses, and p-values for analyses of variance under the null hypothesis of no sig-nificant difference among numbers of specimens or diversity with depth are also shown. All measure were log-transformed prior to the analysis of variance. Values of G250 could not be calculated for faunules comprising fewerthan 250 specimens, so the number of faunules used to calculate statistics for G250 are shown as n250.

Water depth n N G � H n250 G250

�50 m 12 5532 (1861) 120.2 (20.2) 25.3 (2.95) 3.07 (0.170) 10 50.2 (4.67)51–101 m 6 2241 (712) 133.8 (25.9) 33.8 (6.24) 3.37 (0.264) 5 64.3 (7.7)

101–500 m 5 4446 (1420) 180 (22.47) 39.1 (3.03) 4.06 (0.110) 5 74.5 (3.82)— p � 0.45 p � 0.25 p � 0.07 p � 0.01 p � 0.02

from a mixture of local communities, each ofwhich follows a log-series distribution butwith different values of �. If the latter is thecase, the difference between values of x esti-mated for fossil and Recent faunules suggeststhat Recent faunules are more likely to includea mixture of shells derived from multiple localcommunities so that spatial heterogeneity isrelatively higher in the Recent than in the fos-sil habitats.

All of the diversity measures are correlatedwith each other, which is not surprising be-cause they are all indices designed to describeaspects of the number of taxa and distributionof taxon abundances within an assemblage. Todetermine whether the relationships amongthe measures of diversity differed betweenfossil and Recent faunules, we fitted a seriesof linear models among pairs of log-trans-formed measures with fossil or Recent codedas a dummy variable. In all cases, the differ-ence in slope estimated for the relationshipamong diversity measures estimated for fossiland Recent faunules was not significantly dif-ferent than zero. Therefore there is no differ-ence in the relationship among diversity mea-sures for fossil and Recent faunules, suggestingthat comparisons of the two sets of faunulesare not biased by differences in taphonomy orsampling methodology.

Variation in Diversity and Abundance withDepth. Diversity increased significantly withinferred water depth (Fig. 3). We evaluatedstatistically the variation in abundance and di-versity with depth using only Pliocene faun-ules with excellently preserved mollusks thatcontain an adequate representation of samplesfrom all three of the depth intervals (Table 3).Such data were not available from older oryounger deposits (Table 2). For the Pliocene

faunules, there was no significant difference inmean abundance or unrarefied taxonomicrichness (G) of faunules from different waterdepths. However, rarefied taxonomic richness(G250) and H increased significantly with in-creasing water depth and �, too, increasedwith depth, albeit with slightly lower statisti-cal significance (p � 0.07). These results sug-gest that at least in the Pliocene, shallow-waterassemblages are less diverse than deeper-wa-ter assemblages. This pattern of decreasing di-versity with depth is related to increased nu-merical dominance of one or a few taxa in as-semblages recovered from shallow-water de-posits. Examination of the distribution of theproportional abundance of the most abundanttaxon in each faunule indicates that super-abundant taxa are more common in faunulesdeposited in water depths less than 100 mthan in faunules deposited in water depthsgreater than 100 m (Fig. 5). On average, themost abundant taxon in faunules deposited inshallow or intermediate water comprises 18–25% of the specimens constituting that faun-ule. In contrast, the abundance distribution offaunules deposited in water depths greaterthan 100 m is more even, with on average 10%of the shells from the most abundant taxon inthese faunules. In addition the scatter of max-imum proportional abundance is much largerfor faunules deposited in shallow or interme-diate water depths. Clearly, the accurate esti-mation of diversity from fossils recoveredwithin the range of shelf -depth facies requirescareful sampling because of local patchinessof superabundant taxa.

Temporal Variation in Diversity and Abun-dance. There is negative correlation betweenfaunule age and faunule diversity for all faun-ules when diversity is estimated by � or G250


FIGURE 5. Box plots illustrating the distribution of max-imum proportional abundance in faunules deposited inshallow (�50 m), intermediate (51–100 m), and deep(101–500 m) water facies. The range of each box extendsfrom the first to the third quartile of the distribution andthe median value is indicated. The whiskers associatedwith each box extend to the most extreme data point thatis no more than 1.5 times the inter-quartile range fromeach box. Superabundant taxa are much more rare infaunules interpreted as being deposited in deeper waterthan in faunules deposited in water less than 100 mdeep.

TABLE 4. Kendall’s correlations between faunule diversity and faunule age calculated for all faunules and for shal-low-water faunules only. Correlations were also estimated for diversity of bivalves and gastropods within shallow-water faunules. The number of faunules (n) in each analysis is included, and p-values resulting from a test of thenull hypothesis that the correlations are equal to zero are shown in parentheses. The number of faunules for whichG250 could be estimated is indicated as n250.

Waterdepth Taxa n G � H n250 G250

All All 78 0.021 (0.791) 0.175 (0.023) 0.094 (0.220) 68 0.174 (0.036)�50 m All 49 0.043 (0.665) 0.244 (0.013) 0.155 (0.117) 41 0.286 (0.008)�50 m Bivalves 49 0.327 (0.002) 0.505 (2 � 106) 0.458 (2 � 105) 40 0.579 (8 � 107)�50 m Gastropods 49 0.207 (0.0519) 0.051 (0.629) 0.093 (0.381) 26 0.006 (0.964)

but not H (Table 4, Fig. 3). However, this resultis likely biased by the uneven distribution ofsamples from the full range of water depthsacross all time intervals (Table 1). If the anal-ysis is restricted to faunules from shallow wa-ter, then, using a sequential Bonferroni pro-cedure (Rice 1989; Cabin and Mitchell 2000),we find that the correlations between � or G250

and age become stronger and remain statisti-cally significant even after correction for mul-tiple comparisons of p-values. Similar testscould not be performed for faunules repre-senting deep or intermediate-depth water be-cause they are more patchily distributedacross time and space than shallow-waterfaunules (Table 2). Among the 48 fossil faun-ules, 26 are categorized as shallow, 12 as in-

termediate, and ten as deep; and among the 30Recent faunules only seven come from inter-mediate depths, the remainder being fromless than 50 meters. Because of this disparityin sampling intensity we decided to focus ouranalyses of diversity change on the shallow-water faunules. For shallow-water faunules,there was strong correlation between faunuleage and bivalve diversity (Fig. 6) but not be-tween age and diversity of gastropods (Fig. 7).The p-values associated with tests of null hy-potheses of no significant correlation betweenage and diversity are sufficiently low to re-main significant even following Bonferronicorrections (Table 4). This suggests that thesignal of increasing diversity observed in themore inclusive (‘‘all faunules’’ and ‘‘all taxa’’)analyses was caused by a strong pattern in thebivalves. We also analyzed the distribution ofdiversity in fossil and Recent assemblages tobetter constrain the temporal pattern of diver-sity change with respect to the Pliocene/Pleis-tocene ecological and environmental transi-tion in the southwest Caribbean (Jackson andBudd 1996). The results parallel the correla-tion analysis in that a strong signal of in-creased post-Pliocene diversity in bivalves(Table 5) is masked if data are included fromall water depths and all taxonomic groups.

Regional Diversity and Abundance. Regional(gamma) and between-faunule (beta) diversi-ty was studied to determine how an increasein average local diversity scaled to the region-al level. Examination of cumulative collector’scurves for assemblages obtained by mergingfaunules into a set of stratigraphic bins sug-gests that estimates for G, �, and H are allhigher in the Recent faunules than in the faun-ules recovered from the fossil record (Fig. 8).


FIGURE 6. Plots showing the number of shells and diversity of the bivalve component of shallow-water faunules(�50 m). A, The number of bivalve specimens recovered from each faunule (N). B, The total number of bivalvegenera and subgenera found within each faunule (G). C, Median number of genera and subgenera of bivalves re-corded in each faunule after repeated subsampling of 250 specimens at random (G250). D, Fisher’s � for bivalves. D,Shannon’s H estimated for the bivalve component of each faunule.

However, there is no significant difference inG, �, or H between fossil and Recent regionalassemblages that have been sample standard-ized to 8000 specimens (Fig. 9). Notably, re-gional Fisher’s alpha is almost constant for bi-valves over approximately 7 Myr, from the 11–

8.3 Ma to the 3.4–2.2 Ma bins. Recent regionaldiversity is very similar among sampled sub-regions and significantly higher than for anyfossil bins. Shannon’s H shows a similar over-all pattern with Recent subregional bivalve di-versity being significantly higher than for any


FIGURE 7. Plots showing the number of shells and diversity of the gastropod component of shallow-water faunules(�50 m). A, The number of gastropod specimens recovered from each faunule (N). B, The total number of generaand subgenera of gastropods found within each faunule (G). C, Median number of genera and subgenera of gas-tropods recorded in each faunule after repeated subsampling of 250 specimens at random (G250). D, Fisher’s � forgastropods only. D, Shannon’s H estimated for the gastropod component of each faunule.

stratigraphic bin. Within these analyses thereare diversity estimates for some stratigraphicbins that deserve more detailed discussion.

First, each of the diversity measures indi-cated markedly low regional diversity in the

oldest bin (�11 Ma). This contains two faun-ules, one each from silts and muds of the Ga-tun Formation (Canal Basin) and the TuiraFormation (Chucunaque-Tuira Basin). Collec-tions from the Tuira Formation were exten-


TABLE 5. Results of two-sided Kolmogorov-Smirnov tests of variation in diversity of assemblages of mollusks fromfossil and Recent collections are summarized in this table. For each test, the null hypothesis is that there is nodifference in the diversity fossil and Recent faunules. The test statistic (D) is shown for each test, and correspondingp-values are indicated in parentheses. The number of faunules (n) for the full data set and the number of faunulesfor which G250 could be estimated are also shown.

Waterdepth Taxa n G � H n250 G250

All All 78 0.287 (0.0945) 0.175 (0.562) 0.204 (0.373) 68 0.269 (0.158)�50 m All 49 0.239 (0.489) 0.350 (0.0758) 0.316 (0.136) 41 0.426 (0.035)�50 m Bivalves 49 0.552 (0.00118) 0.783 (6 � 108) 0.711 (2 � 106) 40 0.899 (1 � 108)�50 m Gastropods 49 0.403 (0.0380) 0.222 (0.501) 0.244 (0.385) 26 0.316 (0.581)

sively bulk sampled from all visible expo-sures, whereas those constituting the oldestfaunule—the Martin Luther King faunule—ofthe Gatun Formation were obtained fromweathered exposures on a construction site inthe Canal Basin. Without additional samplingof well-preserved material (including verythin-shelled taxa and small aragonitic spe-cies), it is not possible to determine whetherthe apparent low diversity of mollusks fromthe oldest Gatun Formation sediments is realor an artifact of their relatively poor preser-vation. Subsequently, massive new collectionshave been made from newly exposed, un-weathered outcrops, and the molluscan faunasare currently under investigation (Todd un-published data).

Second, Shannon’s H was very low for bi-valves within the early Pliocene bin (5.4–3.7Ma). Three of the four faunules constitutingthis bin are from the Cayo Agua Formation ofthe Bocas del Toro Basin. These three faunulescontain a characteristic suite of common to su-perabundant bivalve taxa that leads to low Hvalues. Notable among these are the super-abundant small corbulids Varicorbula and Car-yocorbula and the glycymeridid Tucetona. Theoverall composition of the faunas and faunulessuggests the dominance of unvegetated sandsand silty sands neighboring occasional sea-grass meadows that contained more even mol-luscan assemblages. The fourth faunule, thatof Quebrada Brazo Seco (Southern Limon Ba-sin) is not rich enough to merit further ex-amination.

Third, diversity was relatively low duringthe early late Pliocene bin from 3.7 to 3.4 Ma.This might be a result of the relative brief du-ration of the bin, but rates of stratigraphic

turnover of the molluscan fauna during thePliocene were probably not high enough tohave a strong influence over these time scales(Jackson and Johnson 2000). More important-ly, all four faunules contain common to abun-dant taxa that are typical of high-energy, shal-low subtidal sand flats and shoals. At the pre-sent day such habitats may be inhabited bysmall numbers of taxa that achieve super-abundance. Among the bivalves are Tucetona,and the crassatellids Crassinella and Eucrassa-tella, while the gastropods are dominated byhighly active shallow-sand burrowers includ-ing the smooth-shelled carnivores Olivella,Prunum, Natica (Naticarius), and Stigmaulax.

As with our previous analysis of local di-versity, the pattern of increased regional di-versity is much more marked in the bivalvecomponent of the fauna (Fig. 10) than in thegastropod component (Fig. 11) or in the com-bined fauna (Fig. 8). Examination of the shapeof the collector’s curves for gastropods only(Fig. 11) suggests that the apparent lack of sig-nificantly increased diversity of the regionalRecent gastropod pool is caused by incom-plete sampling. The gastropod component ofboth fossil and Recent molluscan assemblagesis generally more diverse than the bivalvecomponent (Fig. 9), but during the Pleistocenethere was a major shift in the relative numer-ical dominance of the gastropod and bivalvecomponents of molluscan assemblages in thesouthwest Caribbean. On average there are1.19 gastropod shells for each bivalve shellcounted from the fossil assemblages, but only0.228 gastropod shells for each bivalve shellcounted from Recent assemblages (Table 1).Gastropods are less common in our Recentcollections than in our fossil collections, so


FIGURE 8. Plots of taxon accumulation curves illustrat-ing the effect of additional sampling on generic diver-sity estimates. Each curve represents the pooled assem-blages from faunules deposited in shallow-water facieswithin a set of stratigraphic intervals. The age range ofeach interval (Ma) is shown. Recent faunules weregrouped into three geographic regions prior to analysis.The input order of collections will determine the shapeof the curve (only the endpoint will not vary), so eachplotted curve represents median values of a set of 100curves generated with random input order. The end-point of each curve is shown as a solid circle. A, Genericrichness (G). B, Fisher’s �. C, Shannon’s H.

FIGURE 9. Comparisons of regional diversity (G, Shan-non’s H, and Fisher’s �) from shallow water (�50 m)within stratigraphic and regional bins. For fossil collec-tions, all faunules recovered from shallow water fromwere merged into six stratigraphic bins based on themidpoint of the age range assigned to each faunule. Re-cent faunules dredged from shallow water weregrouped into regional bins. Sample size was standard-ized with bins by repeated random selection of 8000specimen occurrence records from within each bin. Val-ues extend between the 5th and 95th percentiles of 1000replicates, thus indicating the uncertainty within eachmeasure. Values are shown for all taxa and for bivalvesand gastropods. Statistical tests were not attempted be-cause of limited sample size, but a trend of increasingdiversity is apparent when all taxa are included. Thepattern for bivalves indicates a striking increase in allthree measures of diversity during the Pleistocene.

that each gastropod genus or subgenus is rep-resented by 199 shells in the fossil assemblag-es but each extant genus or subgenus of gas-tropod is represented by only 32 shells in theRecent collections. The average abundance ofbivalve taxa also declines by just under one-half from 361 shells per genus in the fossil as-semblages to 183 shells per genus in the Re-cent assemblages, but this change is not nearly

as great as the 83% decline in average abun-dance observed in gastropods.

This change in overall taxonomic structureof molluscan assemblages has consequencesfor sampling because greater sampling effortis required to document adequately the diver-


FIGURE 10. Taxon accumulation curves for bivalve as-semblages from shallow-water faunules. See the captionfor Figure 8 for more details.

FIGURE 11. Taxon accumulation curves for shallow-wa-ter gastropod assemblages. See the caption for Figure 8for a more details.

sity of rich assemblages characterized by lowaverage abundance than is required for as-semblages characterized by few taxa in highaverage abundance. In the current study, wehave adequate sample sizes to estimate the di-versity of the bivalve component of both fossiland Recent assemblages and probably alsoadequate material to estimate the diversity offossil gastropod assemblages. However, be-cause of the marked decline in gastropodabundance we lack sufficient information tofully document the diversity of Recent gastro-pod assemblages. In addition if there has beena post-Pliocene increase in local diversity ofthe gastropods parallel to that observed forthe bivalves, then our sampling is even morecompromised. Therefore, we currently cannot

determine whether or not there was an in-crease in regional diversity in the gastropodassemblages in parallel with the observed in-crease in regional diversity of bivalve assem-blages, and we can say even less about anychange in average diversity of local gastropodassemblages.

For the southwest Caribbean we concludethat bivalve diversity measured at a basinal(100 km) or larger scale increased markedlysometime in the late Pliocene or Pleistocene.Within the isthmian region, fossiliferous de-posits of this age are spatially restricted, andtheir relative stratigraphic positions and agesare still being refined (McNeill et al. 2000; Get-ty et al. 2001). At present we do not have anadequate number of well-dated collections


within this critical interval to determinewhether the observed changes occurred nearthe Pliocene/Pleistocene boundary or later inthe Pleistocene.

One potential confounding factor is the un-even duration of stratigraphic bins. Raup(1972) summarized this potential source of er-ror with the observation that if taxonomicturnover is continuous, then on average weshould expect to record more taxa in longerstratigraphic intervals than in narrower inter-vals. However, the main result reported hereis an apparent increase in the diversity of theregional taxonomic pool in the Recent. TheRecent collections were collected within a fewyears and are likely to represent time-aver-aged samples of a few thousand years at most.If uneven stratigraphic bins were biasing theresults then we would expect to have recov-ered a more diverse regional fauna from thefossil collections, because they were mergedinto stratigraphic bins with a median durationof 1.4 Myr. In addition, there was no signifi-cant correlation (Kendall’s coefficients) be-tween bin duration and regional diversity forthe fossil assemblages.

Beta diversity among faunules within strati-graphic bins ranges from 0.304 to 0.802 (Table2). Within stratigraphic bins, beta diversitygenerally increases with depth. Beta diversityis consistently lower for shallow-water faun-ules than for those deposited at intermediatedepths. On average genera/subgenera arefound within 37–75% of the faunules consti-tuting any one stratigraphic bin and depth in-terval. Within any depth interval there is noclear trend in diversity with time; shallow-wa-ter normalized beta diversity is remarkablyconstant, mostly varying between 0.37 and0.48, with only the value of the �11 Ma bin(0.62) standing out. Only two faunules wereplaced in the �11 Ma bin. As discussed under‘‘Regional Diversity and Abundance,’’ thecontrast in sampled faunal composition be-tween the well-sampled faunule from the Tui-ra Formation and the weathered Gatun For-mation faunule has probably been exaggerat-ed through loss of small and thin-shelled taxain the latter. We think that the apparent ele-vated beta diversity in this stratigraphic bin isprobably an artifact.

A clear increase in bivalve diversity exists atthe faunule scale and at larger basinal or sub-regional geographic scales within the south-west Caribbean, and the change was concen-trated in the latest Pliocene or Pleistocene. Toexplore the ecological guilds involved in theincreased diversity, we studied the distribu-tion of bivalve life habits within faunules ob-tained from shallow-water facies. Examina-tion of the proportions of ecological groups ofbivalves associated with coral reef habitatsshows an increase in both the abundance anddiversity of taxa with these characteristicssince the late Pliocene (Fig. 12). Also, thespread of these values is greater in post-Plio-cene faunules, suggesting that not all faunulesinclude abundant taxa characteristic of reefsettings, but that there is greater heterogeneityamong the abundance distributions fromfaunules that developed in both reef and non-reef habitats. Therefore, we have additionalevidence for increased distribution of reef andcarbonate bank habitats during the Quater-nary (Todd et al. 2002), but also evidence forincreased spatial heterogeneity between thefaunules that is not visible in our beta diver-sity analyses. Greater spatial heterogeneity isconcordant with an increase in the range ofpercentage carbonate values for sedimentssince the late Pliocene (O’Dea et al. unpub-lished data).

Discussion

Diversity, Abundance, and Water Depth. Ageneral decrease in abundance and an in-crease in diversity with depth have been doc-umented for soft-bottom benthic faunules inthe temperate western Atlantic (Hessler andSanders 1967; Rex 1981; Rex et al. 1997; but seeGray 1997; Gray et al. 1997). These studiescompared diversity across a broad range ofdepths (shelf to abyssal habitats), but our pres-ent data set allows us to test whether a similartrend in diversity occurs within shelf habitatsfor Neogene tropical molluscan assemblages.Previously, we were unable to examine thisbecause our collections contained too fewmollusk-rich fossil assemblages from deeper-water facies (Jackson et al. 1999). For Pliocenemollusks from the southwest Caribbean, deep-water shelf assemblages are more diverse than


FIGURE 12. The proportion of ‘‘reef-associated’’ bi-valves in each faunule plotted against midpoint age.This guild of bivalves includes taxa that are immobileand either cemented, boring, or nesting in hard substra-ta. See Todd (2001a) for a full list of ecological charac-teristics used to define this general ecological group. A,Proportion of taxa recorded from each faunule that werereef-associated. B, Proportion of total number of speci-mens in each faunule from reef-associated taxa.

shallow-water assemblages; however, this in-creased diversity is not reflected in raw countsof taxa because abundance of specimens alsodecreases with increasing depth. A strong in-verse correlation between N and paleodepthswamps a weaker positive relationship be-tween G and paleodepth. Shallow and inter-mediate-depth assemblages of mollusks werestrongly dominated by a small subset of taxa,and only 2% of the taxa were represented by50% of the specimens. Deeper-water assem-

blages were more even, and therefore more di-verse.

Studies of large-scale diversity patternsclearly need to consider the distribution of en-vironments sampled. This is especially im-portant for regional studies. For example, ear-ly Pliocene shallowing in the Bocas del ToroBasin resulted in an apparent increase in di-versity as depositional environments shiftedfrom the bathyal to the neritic zone (Collins1993) with an attendant increase in averageabundance per collection. Models for relatingexpected bias in fossil preservation with se-quence stratigraphy have been developed byHolland (2000) and tested empirically byCrampton et al. (2006).

Diversity, Abundance, and Time. There wasan increase in local and regional diversity ofbivalves among shallow-water faunules be-tween the late Pliocene and the Recent. Therewas also a massive increase in abundance ofbivalves compared to gastropods. The relativedecline in gastropod abundance in the Recentwas such that with current sampling we cannotestimate how gastropod diversity changedsince the late Pliocene. An obvious conclusionwould be that these patterns resulted from ataphonomic or sampling bias so that Recentassemblages contained more small, aragonit-ic, or other kinds of shells that are not likelyto be preserved during fossilization or diffi-cult to extract using paleontological samplingtechniques. We reject this hypothesis for thefollowing reasons:

First, both the fossil and the Recent collec-tions were very largely extracted from unli-thified sands and muds using similar proto-cols that are described in detail above. In ad-dition, detailed examination of collectionsfrom �50 m paleodepth across time bins re-veals that small and thin-shelled aragoniticmollusks that are highly susceptible to taph-onomic and diagenetic filtering are generallyexcellently preserved. These include proto-branch bivalves such as Adrana, Lamellinucula,and Saccella, adult rissooid and pteropod gas-tropods, and the larval shells of gastropods,both as isolated protoconchs and attached toteleoconchs. All of these are thin shelled andfrequently only a few millimeters in size. Inmost cases the finest details of shell ornamen-


tation, such as microsculpture, are also pre-served, allowing confident taxonomic identi-fication. Indeed, among all of the fossil faun-ules it is the Pliocene faunules of shallowdepths from the Southern Limon and Bocasdel Toro Basins (together with a few othersfrom older or deeper deposits) that are mostnotable for containing extremely well pre-served assemblages directly comparable withRecent dredged faunas of the region. We candiscount the role of diagenesis or weatheringin producing a systematic decrease in fossildiversity across the Pliocene at collection orfaunule levels.

Moreover, contrary to expecting to recovermore small specimens from Recent samples,we suspect that there is a bias against recov-ering small shells from the Recent due to theloss of fine material during the dredging pro-cess. The dredge we used has a mesh withopenings approximately 2.5 cm in diameter.This mesh typically becomes clogged withfine sediments, resulting in good recovery ofentombed shells, but some winnowing of ma-terial does occur as the dredge is pulledthrough the water. We suggest that smallshells are likely to be undersampled in the Re-cent dredge samples, and that our estimates ofdiversity from Recent faunules are likely to below. A test of this hypothesis would require awell-designed new sampling campaign in-volving a large number of small-scale samples(box cores or grab samples) from a range ofRecent habitats. Until these data become avail-able we suggest that our results here are con-servative, and that the post-Pliocene increasein local diversity of assemblages of molluskswas even greater than we report here.

Could this bias against sampling smallshells in dredge hauls be causing our observeddecline in the relative abundance of gastro-pods in the Recent faunules? For example, aregastropods on average smaller than bivalvesso that they might be disproportionately lostduring the dredging process? In the absenceof detailed size information there are severallines of evidence that can be used to reject thishypothesis. First, in Recent faunules gastro-pods of a size that could not be lost throughthe mesh show much lower relative abun-dances compared to those in late Pliocene

faunules. This suggests that the pattern existsacross gastropod size classes. Second, there isno known mechanism that will remove smallaragonitic gastropods (e.g., by fragmentationor dissolution) at the expense of small arago-nitic bivalves. In fact, one might expect the op-posite. Some bivalves are very thin shelledand fragile and are easily removed from thesampled record of fossil and Recent faunas.Indeed, very thin shelled bivalve taxa such asthe tellinid Merisca or those that are smallsized, such as the venerid Gouldia, can be usedas taphonomic control taxa (Jablonski et al.1997). Exceptionally high abundances of Goul-dia occur in the Recent Nicaragua�9 and Hon-duras�3 faunules and abundant specimens ofMerisca are present in Nicaragua�10 and SanBlas�7. Excellently preserved specimens of thesame genera have been recovered in muchlower abundances from well preserved Plio-cene faunas from the Cayo Agua and Escudode Veraguas Formations. This marked shift inabundance of some small bivalve taxa (as wellas larger taxa such as Arca, Chione, and others)through time strongly suggests that the mas-sive change in relative abundance of bivalves/gastropods across time is not an artifact ofsampling.

Spatial Scale, Sampling, and Diversity. Theobserved increase of diversity in Recent as-semblages of bivalves in shallow water is like-ly to be a result of increased carbonate habitatand decreased surface productivity as the in-fluence of seasonally cool, nutrient-rich up-welling water waned and the Caribbean wasincreasingly influenced by warm oligotrophicwater amenable to carbonate production (Col-lins et al. 1996b; O’Dea et al. unpublisheddata). But how did an increase in the avail-ability of carbonate-dominated habitat resultin increased local and regional diversity? Onepossibility is that beta diversity increased at aspatial scale that cannot be detected using ourfaunule-level analysis. We would expect thisbecause many reefal molluscan taxa areknown to have highly localized distributions,both those living in soft and in hard substrata(Schlacher et al. 1998; Bouchet et al. 2002). Sur-prisingly, we find no evidence for elevatedbeta diversity at the scale of faunules. One rea-son may be that our faunules are fairly coarse-


scaled, especially in the Recent where sampleswere obtained from dredging transects thatmay cumulatively amount to several kilome-ters in length. Such sampling would have in-evitably mixed various small-scale habitats.Patchiness on the scale of tens of meters is welldocumented in Recent carbonate-dominatedhabitats (e.g., Cochinos Cays [Ogden and Og-den 1998]; Bocas del Toro [Best and Kidwell2000]; San Blas [Andrefouet and Guzman2005]) and it is evident from their taxonomiccompositions (Appendix) that the Recentsamples included here are mostly mixtures ofshells from a range of these patchy habitats.Besides, dredge transects could not be sam-pled on the hard-bottom or shallow reefpatches, but instead were recovered from soft-sediment habits directly adjacent to reefslopes. Therefore, the recovered samples arelikely to have included sediment and faunalelements transported down the reef slopes asdebris. We think that the generally high alphadiversity of the Recent faunules is likely a re-sult of both the highly local distribution ofmollusk taxa in space (and time) and furthermixing of their distributions through dredg-ing. This scale of habitat patchiness could notbe studied at the scale of our faunules. Instead,a large-scale grab sampling or box-coring pro-gram would be essential to estimate and ef-fectively pull apart diversity patterns at thesefine ecological scales (Ellingsen 2002).

A question that arises from our combinedanalysis of Recent and fossil samples iswhether those faunules are sampling diversityat comparable temporal scales? Although theecological scale of the faunules is as similar aspossible, fossil faunules are likely to have ac-cumulated across much greater periods oftime than Recent faunules. Recent shallow-shelf sampled shells can be up to several thou-sand years but most are less than 500 years old(Meldahl et al. 1997; Kidwell et al. 2005). Fur-thermore the majority of the fossil faunules in-clude multiple shell beds—each of whichprobably involved as much time-averaging asany Recent dredged faunule. In addition,taphonomic study of Recent mollusk shellsfrom San Blas indicates that dead shells arebioeroded and dissolved faster in carbonatethan in siliciclastic settings (Kidwell et al.

2005). Therefore, in general we might expectmollusk samples from reefal environments tobe less time-averaged and show reduced di-versity compared to those from coeval silici-clastic facies. Again, this indicates that our Re-cent shallow-water diversity estimates arevery likely conservative. We suspect that iftime-averaging of the Recent faunules, whichare proportionately more carbonate-rich(O’Dea et al. unpublished data), was compa-rable to that within fossil faunules, then ourestimates of Recent species richness and di-versity would be higher still because a greaternumber of both common and rare specieswould be sampled.

Other Biota. Different taxa exhibit highlyvariable and distinct trends in diversity overtime. We have confirmed the results of a pre-vious fossil-only analysis that showed diver-sity of mollusks to be virtually constant overat least 10 Myr from the middle Miocene tolate Pliocene (Jackson et al. 1999). However, re-analysis after addition of Recent collectionsindicates a significant increase in local and re-gional molluscan diversity in the past twomillion years. This may have coincided withor have been consequent upon a major pulsein extinction between 2 and 1 Ma rather thanresulting from an increase in origination ratessince approximately 4 Ma that allowed newtaxa to accumulate over a longer interval, cul-minating with the observed increase follow-ing a million-year sampling gap in the Pleis-tocene (Jackson and Johnson 2000; Todd et al.2002). The timing of regional extinction andthe large-scale ecological changes is still poor-ly constrained (Jackson and Budd 1996), butboth may have been triggered by changes intemperature (Stanley and Campbell 1981; Pe-tuch 1982; Stanley 1986) or planktonic pro-ductivity (Woodring 1966; Vermeij 1989, 2001;Jones and Hasson 1985; Vermeij and Petuch1986; Allmon et al. 1993, 1996; Allmon 2001;Todd et al. 2002) among other factors. Whatseems clear from considering a wide range oftaxa is that there was no significant faunalturnover immediately following the completeclosure of the Central American Seaway at3.5–3.0 Ma (Collins and Coates 1999b). Acrossmajor taxonomic groups so far studied, thechanges in diversity of assemblages of benthic


foraminifers in the southwest Caribbean mostclosely parallel that shown by mollusks,though a late Neogene extinction peak is lack-ing. Species diversity increased from the Mio-cene to the Recent with the addition of speciesknown to characterize carbonate shoal andreef environments at the present day (Collins1993, 1999). Much of the cross-shelf increase indiversity and abundance of carbonate-diag-nostic assemblages occurred sometime be-tween the early Pleistocene and the Recent(Collins 1999), a pattern concordant with theabundance and distribution of carbonategrain types in sediments (O’Dea et al. unpub-lished data). More limited analyses of cheilos-tome bryozoans indicate that, in comparisonto mollusks, they may have become substan-tially more diverse over the past 4 Myr (Chee-tham et al. 1999). Lastly, in contrast to bothmollusks and benthic foraminifers, zooxan-thellate coral diversity remained constant fol-lowing a middle Miocene diversification, butthere was a sharp decrease in coral diversityfollowing a late Pliocene/early Pleistocene ex-tinction (Budd et al. 1994, 1996). This extinc-tion resulted in a marked ecological shift fromsmall free-living taxa characteristic of soft-bottom habitats to dominance of larger reef-building species (Budd and Johnson 2001;Johnson et al. 1995). This suggests that zoox-anthellate coral diversity was more sensitiveto the late Neogene environmental transitionand that patterns of coral diversity are out ofphase with the diversity of the remaining ben-thic biota.

Ecological Effects of Plio-Pleistocene Reef De-velopment. Increased Plio-Pleistocene reef de-velopment has had a major effect on regionalmolluscan diversity. This is because reef sys-tems—including their associated soft substra-ta—are the most species-rich marine ecosys-tems. Many taxa have highly elevated, and of-ten their highest, diversity on reef systems(Peterson 1979; Done et al. 1996; Paulay 1997),but this biotic diversity is manifested at dis-tinct spatial and ecological scales. Reefs them-selves are characterized by high biologicalproductivity, are spatially heterogeneous, andcomprise architecturally diverse substrata.The varied architecture maintained by the bal-ance of reef constructors and eroders in turn

supports large populations of herbivores, de-tritivores and carnivores that show fine-scalepartitioning of habitat and food. Hence, eco-logical interactions and food webs in reef sys-tems are typically more complex than those oflevel-bottom communities. Mollusks are thenumerically most diverse reef-dwelling ani-mals likely to be preserved as fossils, and taxawith specialized and coevolved feeding habitsare particularly species-rich in these habitats(Paulay 1997; Bouchet et al. 2002). For exam-ple, within a single extant reef, highly diverseand trophically specialized gastropods in-clude feeders upon cnidarians and sponges(e.g., Ptenoglossa: Epitoniidae, Cerithiopsi-dae, Triphoridae), parasites and grazers on arange of metazoans (Eulimidae, Pyramidelli-dae) (Bouchet et al. 2002), and specializedpredators on polychaetes and fish (e.g., Con-oidea [Kohn 2001]), as well as diverse bivalveclades including those living in symbioseswith other invertebrates (Galeommatoidea)(Bouchet et al. 2002). Many of these familiesare poorly known as they have small body siz-es (modal shell size for species on a tropicalIndo-Pacific reef is 3 mm) and cryptic life-styles so are often overlooked in Recent (andwe suspect many fossil) sampling programs(Reaka-Kudla 1997; Bouchet et al. 2002).

In addition to the highly elevated diversityof reefs, associated soft-substrate ecosystemsmay harbor species-rich molluscan commu-nities that are distinct from those within non-vegetated level-bottom faunas. From the Plio-Pleistocene onward, fringing reefs have beenthe dominant reef type in the southwest Ca-ribbean (Budd et al. 1999; Spalding et al. 2001)and here, as elsewhere, they are critical forsheltering and facilitating the accumulation ofback-reef seagrass meadows and landwardfringes of mangrove. These three componentsare intimately linked both in terms of the gen-esis of the wider reef system and its sedimen-tation patterns (McCoy and Heck 1976) andchemically through nutrient transfer (Ogden1997). It is probable that the widespread de-velopment of coral reef systems in the Plio-Pleistocene, the first in the region since theirdemise in the early Miocene (Vaughan 1919;Johnson and Kirby 2006; Johnson and Jacksonunpublished data), was implicated in a con-


comitant late Neogene increase in shallow, de-tritus-based seagrass meadows such as thoseformed by Thalassia today (Domning 2001).These have characteristic and sometimes high-ly diverse molluscan communities containingrich faunas of snails grazing on epiphytes anddetritus on living seagrasses (e.g., rissooidand cerithioid snails [Heck 1977; Bitter-Soto1999; Hill 2002]) and infaunal, chemosymbiot-ic bivalves (Lucinidae) (Jackson 1973).

High-diversity, reef-associated seagrass as-semblages are known from horizons aroundthe Plio-Pleistocene transition (e.g., the MoinFormation, Southern Limon Basin [Todd andCollins 2006]) and may be similar to those inthe region today (Domning 2001). In contrast,older assemblages containing microgastro-pods consistent with a seagrass environmentare present, for example, in the late Miocene(within the Gatun Formation) and the Plio-cene-aged Cayo Agua Formation (Todd un-published). These were probably not associ-ated with reef buildups, and paleobathyme-tric estimates obtained from benthic foramin-ifers (Collins 1999; Collins in Jackson et al.1999) suggest that at least some pre-transitionseagrass habitats formed at greater depthsthan reef-associated seagrass meadows withinthe Caribbean today (Cheetham and Jackson1996).

The fauna of the Florida Keys is much betterknown than that of most reefal environments,yet recent studies have more than doubled thespecies richness of its bivalve fauna and haveemphasized its dissimilarity in taxonomiccomposition to nearby regions (e.g., Cuba,Gulf of Mexico) (Mikkelsen and Bieler 2000).However, to date, no complete biotic invento-ries exist for any reef in the Caribbean or else-where (Reaka-Kudla 1997), and remarkablythe only in-depth sampling of molluscan di-versity across a wide variety of reef systemhabitats yet published is that of Bouchet et al.(2002) in New Caledonia (tropical Indo-Pacif-ic). Nevertheless, more -limited surveys indi-cate that a large proportion of Recent marinebiodiversity in the tropical Western Atlanticmay be associated with reef systems (Paulay1997). Our results suggest that much of thisdiversity, at least in the southwest Caribbean,is geologically young (Jackson and Budd 1996)

and its growth was driven by the developmentof substantial coral reefs within the past 2Myr.

Implications for Large-Scale PaleodiversityStudies. Our results emphasize that shallowshelf sediments most frequently preservedand sampled in the fossil record may showlarge variations in species richness and even-ness over small spatial and temporal scales. Itis known that patchiness, rarity, and local en-demism in today’s tropical reefal environ-ments—where marine diversity is highest—may be extreme (Schlacher et al. 1998; Bouchetet al. 2002). Recent molecular phylogeneticstudies of large, conspicuous, and apparentlywell-known reefal mollusk taxa have revealedabundant semi-cryptic species-level diversifi-cation and high degrees of endemism overmodest geographic distances in the Caribbean(Todd and Rawlings 2003; Lee and O’Foighil2004) and elsewhere. These patterns areshown by organisms as diverse as snappingshrimp (Morrison et al. 2004) and reef fish(e.g., Ruber et al. 2003; Taylor and Hellberg2005); indeed, they appear to be pervasiveamong reef-associated organisms worldwide(Meyer et al. 2005). The extant diversity ofreef-dwelling organisms is likely to be under-estimated by an order of magnitude and thereis no reason not to suspect that similar levelsof diversity existed in the past. In this study,we have shown that there was a significantpost-Pliocene increase in generic diversity ofbivalve assemblages in the southwestern Ca-ribbean, but we did not have sufficient infor-mation to detect a similar change in the di-versity of gastropod genera. Clearly, to obtainrobust measures of diversity at species orhigher levels in tropical macrobenthic groupssuch as mollusks requires large-scale, stan-dardized ecological sampling where speci-men abundance is recorded; otherwise, abun-dance and diversity will remain conflated. Justas shown by Recent ecological sampling pro-grams (Ellingsen 2002) (1) water depth andsubstrate are key correlates of Neogene mol-luscan diversity at the local level, and (2) thearchitectural and habitat complexity of tropi-cal reefal systems harbor elevated local andregional diversity of mollusks and other fos-silizable taxa. To better understand the timing


and tempo of molluscan (and other faunal) di-versity increase within the region during thepast 2 Myr it is critical that we sample morecollections from this interval, and in particu-lar those dating to the last 1.4 Myr. A combi-nation of new assemblage data with combinedfossil and molecular phylogenetic studies ofselected species-rich clades (e.g., Todd andRawlings 2003) has great potential to revealthe ecological context of diversity increaseduring the Plio-Pleistocene.

Acknowledgments

Many colleagues assisted with the field-work, collections curation, taxonomic identi-fications, and compilation of the geologicaland paleontological data used in this study,including M. Alvarez, A. Coates, L. Collins, H.Fortunato, A. Heitz, P. Jung, D. Miller, R. Pan-chaud, J. Smith, F. Wiedermeyer, and the crewof the R/V Urraca. Collections of fossil spec-imens are reposited at the NaturhistorischesMuseum Basel, and collections of Recent mol-lusks are held by the Smithsonian Institution.A. Clarke, J. Crampton, and S. Connolly pro-vided detailed and insightful reviews of thetext. We acknowledge the support of the U.S.National Science Foundation (BSR90-06523,DEB-9300905, DEB-9696123, DEB-9705289,EAR-9909485 and DBI-0237337), the U.K. Nat-ural Environment Research Council (NERGR3/13110), Kuglerfonds of the Naturhisto-risches Museum Basel, National GeographicSociety, Scholarly Studies and Walcott Fundsof the Smithsonian Institution, Schweizerisch-er Nationalfonds Forschung (21-36589.92 and20-43229.95), Natural History Museum Lon-don, Naturhistorisches Museum Basel, andthe Smithsonian Tropical Research Institute.

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