Palaeontologia Electronica · 2014-11-23 · PALAEO-ELECTRONICA.ORG 3 analysis and hypothesis testing (Stigall Rode 2005). Biogeographic patterns are controlled by a combination of

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USING GIS TO ASSESS THE BIOGEOGRAPHIC IMPACT OFSPECIES INVASIONS ON NATIVE BRACHIOPODS

DURING THE RICHMONDIAN INVASION IN THE TYPE-CINCINNATIAN(LATE ORDOVICIAN, CINCINNATI REGION)

Alycia L. Stigall

ABSTRACT

The Late Ordovician age strata in the Cincinnati, Ohio, region record a dramaticimmigration of exta-basinal taxa into the region, termed the Richmondian Invasion, atthe Maysvillian/Richmondian Stage boundary. The effects of the species invasion ongenus-level paleoecology and biodiversity are well characterized; however, no prioranalyses have examined biogeographic patterns in terms of areal extent of geographicranges at the level of individual species at fine spatial or temporal scales. Geographicranges of rhynchonelliform brachiopod species and genera were reconstructed usingGIS-generated bounding polygons for each of the six depositional sequences delin-eated within Cincinnatian strata in order assess biogeographic patterns before, during,and after the Richmondian Invasion. Taxa were divided into four groups for analyses:native species that become extinct in the Maysvillian, native species that persist intothe Richmondian, new species evolving in the Richmondian from native ancestors, andinterbasinal invaders. Several statistical patterns emerge: native species with largerranges preferentially survive compared to those with smaller ranges; carryover taxaexhibit no significant change in range size following invasion; both carryover andinvader taxa exhibit large geographic ranges characteristic of eurytopic taxa, whereasnew species have small ranges and are ecological specialists. Invasive species, there-fore, most profoundly impacted narrowly adapted, specialist species during the earlystages of invasion. Ecosystem response to the invasion continued for at least one mil-lion years. Native generalist taxa occupied larger geographic ranges than invader taxafor the first million years of the invasion, indicating a limited role for competition in driv-ing ecosystem change.

Alycia L. Stigall. Department of Geological Sciences and OHIO Center for Ecology and Evolutionary Studies, Ohio University, 316 Clippinger Laboratories, Athens, Ohio 45701 USA [email protected]

Keywords: Ordovician, paleoecology, speciation, extinction, Katian

INTRODUCTION

The highly fossiliferous Upper Ordovician

units exposed along the Cincinnati Arch in south-western Ohio, northern Kentucky, and southeast-ern Indiana comprise the type strata for the

PE Article Number: 13.1.5ACopyright: Paleontological Society March 2010Submission: 22 July 2009. Acceptance: 27 January 2010

Stigall, Alycia L., 2010. Using GIS to Assess the Biogeographic Impact of Species Invasions on Native Brachiopods During the Richmondian Invasion in the Type-Cincinnatian (Late Ordovician, Cincinnati Region). Palaeontologia Electronica Vol. 13, Issue 1; 5A: 19p; http://palaeo-electronica.org/2010_1/207/index.html

STIGALL: CINCINNATIAN BIOGEOGRAPHY

Cincinnatian Series (Figure 1; Davis and Cuffey1998). These strata are well known for their tre-mendous abundance of fossils, faunal diversity,and high quality of preservation. The fossils of theCincinnati region have been studied for over 150years, and major patterns of faunal turnover, com-munity structure, and paleoecological gradientshave been well characterized. Large-scale paleo-biogeographic patterns, particularly as they pertainto either origination of the Cincinnatian fauna or

paleoecological gradients, have been examined.However, no quantitative analyses of paleobiogeo-graphic patterns at the species level have yet beenpublished. In this paper, the paleobiogeographicranges of rhynchonelliform brachiopod species andgenera of the type Cincinnatian strata are recon-structed and quantified.

Quantitative paleobiogeographic analyseshave the potential to provide new insights into pat-terns of faunal turnover by facilitating statistical

FIGURE 1. Data distribution by sequence mapped onto the Cincinnatian outcrop belt. The outcrop belt is a structuralarch; therefore, the central region exposes Middle Ordovician units and strata become progressively younger awayfrom the central region.

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analysis and hypothesis testing (Stigall Rode2005). Biogeographic patterns are controlled by acombination of both evolutionary and ecologicalfactors (Lomolino et al. 2006). Consequently, bio-geographic assessments can provide detailedinformation about the impact of environmentalchanges (both biotic and abiotic) on faunal dynam-ics (Stigall 2008). Within the Cincinnatian strata, asignificant interval of faunal immigration, termedthe Richmondian Invasion, is associated with thetransition between the Maysvillian and Richmon-dian Stages (Holland 1997). In this study, the bio-geographic impact of the introduction of theinvader taxa on native brachiopods is analyzed.Specifically, the long-term effects of communityrestructuring previously identified during this inter-val (Holland and Patzkowsky 2007) are assessedas they pertain to biogeographic patterns andniche breadth.

Modern invasive species have been known tosignificantly disrupt ecosystems into which they areintroduced. Most modern invasive species occur innew ecosystems due to human activity (Davis2009), either through intentional introductions(such as song birds or cultivated plants thatbecome naturalized) or inadvertently (such asstowaways on cargo ships). The term invasion has,however, also been used to describe any processof dispersal and establishment beyond a formerrange for modern species (Reise et al. 2006). Spe-cies invasions in the fossil record occur due to nat-ural causes, for example a relative rise in sea levelthat leads to breaching of geographic barriers orremoval of oceanographic barriers (Vermeij 2005).Therefore, for a fossil species to be consideredanalogous to a modern invader, it must haveevolved in one geographic region or tectonic basinand then subsequently immigrated into a secondregion in which it did not evolve (Stigall 2010).These species have similar impacts to moderninvasive species because they are newly intro-duced to ecosystems with which they did notevolve in concert.

The impact of these invaders (fossil or mod-ern) is expected to include increased competitionfor resources and increased predation on nativetaxa (Lockwood et al. 2007; Davis 2009). Theeffect of increased predation is well characterizedfor modern invasive species: the introduction ofnovel predators often results in local extinction ofprey species (Davis 2009). For example, the intro-duction of the Brown Tree Snake has decimatedthe endemic species of ground-nesting birds inGuam (Fritts and Rodda 1998). The long-term

effects of increased competition, however, areunclear. To date, no studies of modern invasivetaxa have successfully demonstrated completeextinction of native species due to competition frominvaders (Davis 2003). Studies of invasion biology,however, are limited in temporal duration. Fieldstudies typically are conducted over several years,and even the best-studied historical invasions havean observational record of only decades. Longerterm patterns inferred from invasion events in thefossil record, therefore, have the potential to pro-vide insight into the long-term impacts of speciesintroductions.

Cincinnatian strata that preserve the geo-graphic distribution of species before, during, andafter the Richmondian Invasion provide a naturallaboratory to test patterns of species level and eco-system response to species invasions over geo-logic time. This paper expands on previous studiesof community organization across the invasioninterval (e.g., Holland and Patzkowsky 2007) byanalyzing patterns of biogeographic distribution atthe species level. In particular, the impact of theRichmondian invasion on native taxa is assessedby examining temporal shifts in geographic rangesof species within species groups. The differentialresponse of native species that adapted success-fully to the invasive regime versus those that didnot can thus be ascertained. Furthermore, the tim-ing of invasion impact is investigated by analyzingbiogeographic patterns in each of six depositionalsequences separately. This study, thereby, pro-vides insight into the long-term effects of invasivespecies in modern ecosystems. This is particularlysignificant because the longer term effects of bioticinvasions on these issues cannot be studied overecological timescales.

GEOLOGIC SETTING AND STRATIGRAPHY

During the Late Ordovician, the Cincinnatiregion was located nearly 20 degrees south of theequator and rotated 45 degrees clockwise from itspresent orientation (Figure 2) (Scotese and McKer-row 1991). The Cincinnati region occupied a distalposition in the Taconic foreland basin, developedfrom the collision of an island arc system with theeastern seaboard of Laurentia (Brett and Algeo2001). The study area assumed a ramp structurewhich gently dipped from the modern southeast tonorthwest and was covered by a shallow epiericsea up to 30 m deep (Holland 2008).

Strata of the type Cincinnatian Series aredivided into six depositional sequences, C1 to C6(Figure 3) (Holland 1993; Holland and Patzkowsky

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1996). Each sequence spans between approxi-mately three quarters of a million years to two mil-lion years. Thin transgressive systems trackdeposits occur at the base of the sequences, butthe majority of the sequences represent highstanddeposition. Each sequence records an overall shal-lowing upward progression, and the sequencesshallow upward overall due to infilling of the basin.

Four primary depositional environments werearrayed along the ramp: offshore, deep subtidal,shallow subtidal, and peritidal (Holland 1993,2001). Sedimentology varies with paleoenviron-ment, but in general, Cincinnatian sediments repre-sent storm-derived deposition (Brett and Algeo2001). Layers alternate between terrigenous mud-stones comprising sediments sourced from theweathering Taconic highlands and bioclastic pack-stones to grainstones, which represent the shellystorm lag (Jennette and Pryor 1993). In deeper-water paleoenvironments, mudstones comprise ahigh percentage of the section as only the largest

storms were able to disturb the seafloor sediments,whereas shallower water deposits are dominatedby limestone layers because the fine-grained parti-cles were almost entirely winnowed away bystorms or waves (Jennette and Pryor 1993; Hol-land 2001). Although storm processes were perva-sive in the Cincinnatian system, lateral transport ofskeletal debris was limited (several meters) as evi-denced by the ability to resolve detailed paleoeco-logical changes within limestone units at theoutcrop scale (Frey 1987; Barbour 2001).

In general, Cincinnatian limestones lack fea-tures associated with tropical deposition (e.g.,ooids, peloids, and significant micrite) and exhibitcharacteristics of cool-water carbonates. Becausethese layers were deposited in the paleotropics,they are interpreted to represent a high-nutrientsystem rather than truly cool-water deposition (Hol-land and Patzkowsky 1996). This is particularly thecase for the C1 to C4 units. These units containphosphate grains and crusts indicative of high-

Source of invaders

T

A

Laurentia

Baltica

0°

30° S

FIGURE 2. Paleogeographic reconstruction of Laurentia in the Late Ordovician. The star indicates the Cincinnatiregion. Most of Laurentia is covered by a shallow epicontinental sea. The Taconic foreland basin extends to the southof the study region. A: Transcontinental Arch, T: Taconic Highlands.

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nutrient conditions (Holland 2008). In the C5 andC6 sequences, phosphate deposition decreases,nutrient levels appear to drop, and micritebecomes more abundant. This shift in nutrient loadhas been interpreted as a shift in paleooceano-graphic conditions (Holland and Patzkowsky1996). This shift appears to coincide with the Rich-mondian transgression and the influx of invadertaxa into the basin, as discussed more fully below.

PALEOECOLOGICAL FRAMEWORK

Cincinnatian strata preserve a rich anddiverse fauna. Even though graptolites, conodonts,and nautiloids occur, the preserved fauna is pri-marily benthic and is dominated by brachiopodsand bryozoa with associated echinoderms, trilo-bites, gastropods, bivalves, and corals (Feldmann1996; Davis 1998; Meyer and Davis 2009). Numer-ous recent analyses have elucidated aspects ofCincinnatian paleontology including studies ofdiversity structure (Novack-Gotshall and Miller2003), autecology of specific taxa (Leighton 1998;

Datillo 2004), biofacies (Anstey et al. 1987; Bar-bour 2001; Holland et al. 2001; Holland and Patz-kowsky 2007; Patzkowsky and Holland 2007),characterization of ecological and faunal gradients(Miller et al. 2001; Holland et al. 2001; Holland2005; Holland and Patzkowsky 2007), microevolu-tionary patterns (Webber and Hunda 2007), andtaphonomy (Meyer 1990; Brandt-Velbel 1985).

The most dramatic shift in paleoecologicalpatterns occurs across the Maysvillian-Richmon-dian (C3-C4) boundary. The onset of the Richmon-dian Invasion occurs in the C4 sequence when asuite of taxa from the paleoequatorial region immi-grated into the Cincinnati region (Foerste 1917;Holland 1997). Significant faunal reorganizationoccurred during the C4 sequence. Detailed gradi-ent ecology and biofacies analyses of genus-levelcommunity composition by Holland and Patz-kowsky (2007) indicated that the C1 to C3 pre-invasion communities exhibited high levels of simi-larity in community structure. The C4 sequencepreserves a fundamental breakdown/restructuring

C5

C4

C3

C2

C1 Kope

WhitewaterLiberty

Waynesville

Oregonia“Sunset”

Mt. AuburnCorryville

Bellevue

Fairview

Miamitown

LITHOSTRATIGRAPHYSEQUENCE

Ric

hm

on

dia

nM

aysv

illia

nEd

enia

n

Kat

ian

445

446

447

448

449

450

C6 Upper Whitewater444

Ma STAGE West EastNAmIntl

FIGURE 3. Cincinnatian stratigraphy. Modified from Holland and Patzkowsky (1996).

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of biofacies. Clearly differentiated biofacies arereestablished during the C5 sequence, althoughthe C5 community structure differs significantlyfrom those of the Maysvillian due to the ecologicaldominance of many invader taxa (Holland andPatzkowsky 2007).

The Richmondian Invasion was a cross-faunalimmigration event. Taxa new to the Cincinnatiregion included species from all trophic levelsincluding tabulate and rugose corals, nautiloidcephalopods, gastropods, bivalves, trilobites, andbrachiopods (see Holland 1997 for a complete listof invader taxa). The influx of invaders appears tohave been largely unidirectional from the paleoe-quatorial region of the western United States andCanada (Figure 3) and thus was originally referredto as an invasion of the “Arctic Fauna” (Foerste1917). Significantly, the influx of invaders did notresult in an appreciable increase in extinction rate.Instead, many native species persisted across theinvasion interval, resulting in higher diversity levelsin Richmondian units compared to Maysvillianstrata of the Cincinnati region (Patzkowsky andHolland 2007). Particularly notable were the intro-ductions of taxa such as rugose corals and rhyn-chonellid brachiopods. Member of theseorders—and in some cases the same genus (i.e.,Rhynchotrema)—were present in the CincinnatiArch during the Mohawkian Stage, but were absentfor at least five million years prior to their reintro-duction (Elias 1983; Holland 1997). During theinterval of their absence, members of the invadergenera occurred in paleoequatorial waters and arepreserved in strata in Canada and the WesternUnited States. For example, Grewingkia, Strepte-lesma, and Rhynchotrema occur in the SteamboatPoint Member of the Bighorn Dolomite of Wyo-ming, which is correlative with the C2 sequence(Holland and Patzkowsky 2009). Furthermore, cer-tain invader species, such as Thaerodonta clarks-villensis and Hiscobeccus capax, occur in theMaysvillian portions of the Red River Formation ofSouthern Manitoba (Jin and Zhan 2001). Hollandand Patzkowsky (1996) have linked the invasionwith paleo-oceanographic changes that resulted inwarm, low nutrient waters replacing the formernutrient-rich temperate conditions in the Cincinnatiregion, thereby facilitating the migration of paleoe-quatorial taxa into the area.

METHODS

Data Acquisition

For this analysis, biogeographic ranges oftaxa were reconstructed at both the species andgenus level at the temporal resolution of strati-graphic sequence of Holland and Patzkowsky(1996) using Geographic Information Systems(GIS). The geographic ranges of rhynchonelliformbrachiopods were reconstructed because analysesof these organisms are expected to produce themost accurate range reconstructions for Cincinna-tian taxa. Brachiopod fossils are among the mostdiverse and abundant fossils that are present in allCincinnatian depositional environments, and mostcan be identified to species based on external skel-etal morphology (Meyer and Davis 2009). Highsampling density and accurate species identifica-tions reduces undersampling and other errorspotentially associated with range reconstruction(see Rode and Lieberman 2004). Brachiopodslived on or borrowed shallowly within the seafloor,thus their fossils distribution likely reflects theiractual living distribution accurately on the outcropscale (Kidwell and Flessa 1996), the scale at whichthese analyses are conducted. As noted above,storm processes, which affected Cincinnatian ben-thos, did not result in significant lateral transport ofskeletal material (Frey 1987; Barbour 2001). More-over, Finnegan and Droser (2008) noted that stormdeposits have a higher proportion of local taxa thanunreworked beds because they concentrate raretaxa in the resulting lag. Consequently, althoughthese storms impacted the sediment, stormreworking produced biodiversity data that are morecomplete than non-reworked deposits.

Data required to reconstruct geographicranges consist of geographically and temporallyrestricted species occurrence data. These datainclude species identification, precise latitude andlongitude coordinates of the collection locality, andstratigraphic information to place the speciesoccurrence within the correct stratigraphicsequence. Species occurrence data were collectedfrom museum collections, targeted field work, andthe Paleobiology Database (paleodb.org). Collec-tions at the Cincinnati Museum Center, Miami Uni-versity Limper Museum, and the Ohio StateUniversity Orton Geological Museum were exam-ined. At each museum, specimens were inspectedby the author in order to verify (or correct) speciesidentifications. Species identifications followedpublished identification keys (Davis 1998, Feld-mann 1996) and published synonymies (e.g.,

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Walker 1982). Taxa known to be problematic or forwhich current consensus opinion questions theirtaxonomic validity (e.g., Platystrophia unicostataand Rafinesquina fracta ) were excluded from thedatabase. Specimens with stratigraphic or geo-graphic information that could not be resolved tosequence or precise location (e.g., Late Ordovi-cian, Cincinnati Region) were necessarily excludedfrom the dataset. Museum data were supple-mented by a download of data, primarily the data-set of Holland and Patzkowsky (2007), from thePaleobiology Database and field work targeted tofill in gaps in data coverage. The final speciesoccurrence database includes 1490 unique spe-cies occurrence data points for 49 brachiopod spe-cies in 21 genera across all six depositionalsequences (Figure 1, Tables 1, 2, Appendix 1,note: all tables and appendices are available onthe website palaeo-electronica.org/2010_1/index.html).

Range Reconstruction

Geographic ranges were calculated in twoways using GIS. The first method estimates thearea of a geographic range by creating a minimumspanning convex hull to enclose all known occur-rence points for a taxon (see examples in Figure4). Using this method, all known taxon occurrencesites are enclosed by a polygon with the fewestpossible number of sides, then the area of thatpolygon is calculated in ArcGIS (ESRI 2008). Thismethod has been successfully employed withDevonian brachiopods and bivalves (Rode and Lie-berman 2004), Devonian phyllocarids (Rode andLieberman 2005), and Cambrian arthropods (Hen-dricks et al. 2008). Step-by-step instructions for thismethod are presented in Stigall Rode (2005) andStigall (2006). Although the polygon method pro-vides the most parsimonious estimate of a taxon’sgeographic range, it is potentially sensitive tounderestimation of a taxon’s range due to under-sampling or overestimation of geographic rangesthat were not laterally continuous (see Stigall Rodeand Lieberman 2005). Therefore, geographicranges were also estimated using a distancemethod based on the maximum linear extentbetween two points of known taxon occurrence, amethod previously employed by Hendricks et al.(2008). To further reduce the sensitivity of theresults to sampling bias, analyses were calculatedat both the species and genus levels. The 49 spe-cies analyzed comprised 21 genera. Of these,twelve invasive genera and one Maysvillianrestricted genus were monotypic within the study.

There are currently no published phylogeneticanalyses for relationships of Cincinnatian brachio-pods. The monophyly of some genera, such asStrophomena and Platystrophia, have been ques-tioned (Zuykov and Harper 2007; Leighton, per-sonal comun., 2009), while some species, such asDalmenella meeki, are known to be assigned togenera to which they do not belong (Jin, personalcomun., 2009). As species are a primary unit ofevolutionary innovation, whereas genera representsystematists’s opinions of related but potentiallynon-monophyletic groups of species, the discus-sion below will focus primarily on species-level pat-terns. Generic level data will be used to assessand support the relative strength of the pattern atmultiple taxonomic levels.

The areal extent of the outcrop belt shifts sig-nificantly in both size and location amongsequences. As discussed above, Cincinnatianstrata were deposited along a depositional ramp,which prograded northward through time. Further-more, strata are now exposed along a structuralarch. Therefore, the oldest sequences outcropmore centrally along the arch whereas the youngersequences occur both toward the northern andmore distal regions of the arch (Figure 1). In orderto meaningfully compare temporal patterns amongsequences, these variations in outcrop availabilitymust be accommodated. Therefore, calculatedgeographic ranges were normalized by outcropextent for each time slice. Areal ranges were nor-malized by dividing the observed range by the areaof the minimum convex hull digitized for all speciesoccurrence data in the database for a singlesequence (Tables 1, 2, note: all tables and appen-dices are available on the website palaeo-electron-ica.org/2010_1/index.html). Maximum linearextents were similarly normalized by dividing bythe maximum linear extent between any pair ofspecies occurrences within a single sequence(Tables 3, 4, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html).

A second standardizing procedure, dividingthe raw geographic range estimate by the numberof species occurrence points used in the rangeestimation, was also undertaken (Appendix 2).Results of statistical analyses conducted with datanormalized by occurrence points were congruentwith those of the area standardized data. (Appendi-ces 3-4, 6-9). Normalizing by outcrop extent is lessheavily influenced by sampling bias or samplingintensity. Therefore, results of analyses conducted

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8

Ohio

Kentucky

Indiana

Hebertella occidentalis

Platystrophia acutilirata Rhynchotrema dentatum

Dalmanella multisecta

C1

C2

C4

C6

C5

C3

N

0 50 100 km

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

FIGURE 4. Representative species-level paleogeographic reconstructions. (1-6) Range reconstructions for a carry-over species, Hebertella occidentalis in the C1 through C6 sequences, (7-9) Range reconstructions for a Edenian toMaysvillian restricted species, Dalmanella multisecta in the C1 through C3 sequences, (10-12) Range reconstruc-tions for a native descendant species, Platystrophia acutilirata in the C4 through C6 sequences, (13-15) Rangereconstructions for an invasive species, Rhynchotrema dentatum in the C4 through C6 sequences.


using the area standardized range values will bediscussed in the text.

Statistical Analyses

To assess whether certain types of speciesresponded differently to the invasive regime, spe-cies were categorized into four groups: (1) speciesnative to the Cincinnati region which did not persistbeyond the Maysvillian Stage, (2) species native tothe Cincinnati region which were extant in theMaysvillian and carryover into the Richmondian,(3) species that evolved in the Richmondian fromCincinnati natives, and (4) extrabasinal invaders(Tables 1-4, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html). For generic analyses, onlycategories 1, 2, and 4 were used. Because phylo-genetic relationships are almost entirely unknownfor Cincinnatian brachiopods, species group mem-bership was coded in two ways. In the first codingstrategy (indicated in Tables 1-4, note: all tablesand appendices are available on the websitepalaeo-electronica.org/2010_1/index.html), cate-gory 3 includes all Richmondian species assignedto a genus that existed Cincinnati during theMaysvillian, and category 4 includes all Richmon-dian species assigned to a genus absent fromMaysvillian strata of the Cincinnati region. Thiscoding scheme assumes that all of the Richmon-dian members of a Maysvillian genus occur inRichmondian strata due to speciation within thebasin and that none of these species migrated toCincinnati as part of the Richmondian Invasion.While this interpretation is the most parsimonious,it may not be accurate for all species in the cate-gory; some species of native genera may be. Thismay have arrived in the Cincinnati region as part ofthe invasion, particularly true for species of Stro-phomena. This genus is absent from C3 strata ofthe Cincinnati region (Table 1, note: all tables andappendices are available on the website palaeo-electronica.org/2010_1/index.html), which mayrepresent extirpation from the basin. Furthermore,some Richmondian species, notably Strophomenaplanumbona, occur in the Maquoketa Formation onthe west side of the basin during the C3 sequence(Leighton, personal commun., 2009). Therefore, asecond coding strategy was employed in which allRichmondian species of Strophomena weretreated as invasive rather than as native descen-dants. For generic analyses, Strophomena wastreated as a carryover taxon in the first codingstrategy. In the second coding strategy, C1 and C2Strophomena were treated as Maysvillian

restricted genus while the C4-C6 Strophomenawere treated as an invasive genus.

Two sets of statistical analyses were con-ducted based on the estimated geographic ranges.The first assessed differences in geographic rangeversus taxon group; whereas the second set ana-lyzed changes in geographic range by sequence.Differences in geographic response by taxon groupwere analyzed using one-tailed t-tests, and tempo-ral patterns were assessed using analysis of vari-ance (ANOVA). All analyses were conducted withMinitab 15 (Minitab Inc. 2007). Analyses were con-ducted separately for the two taxon group codingstrategies.

RESULTS

Comparison by Group Membership

Geographic range reconstructions for speciesrepresentative of each taxon group are illustratedin Figure 4. Visual comparison of the 95% confi-dence intervals of the mean geographic range ofthe four taxon groups delineated above suggestssignificant differentiation of geographic range sizewithin these groups. Congruent results wereobtained regardless of coding strategy or standard-ization procedure (Figure 5.7, Appendix 5). Aseries of hypotheses related to how taxonomicgroups responded to the invasive regime wereassessed using one-tailed t-tests (Table 5, Appen-dices 3, 6, 8, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html).

Results indicate that among native Cincinna-tian taxa, species or genera that cross over into theRichmondian had statistically larger geographicranges than those that do not (Table 5.1, note: alltables and appendices are available on the websitepalaeo-electronica.org/2010_1/index.html). Spe-cies area, species linear, and generic area analy-ses are highly significant under both codingstrategies. The genus linear analysis is significantat the level of p = 0.096 when Strophomena istreated as native and p = 0.021 when Strophomenais treated as a Richmondian invader. For thosenative taxa that carry over into the Richmondian,geographic ranges are statistically identical at in allanalyses (Table 5.2, note: all tables and appendi-ces are available on the website palaeo-electron-ica.org/2010_1/index.html), indicating that theintroduction of the invader taxa did not produce asignificant range size shift in these taxa. The meanRichmondian range size of carryover taxa is largerthan that of the invasive taxa. When Richmondian

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Strophomena species are coded as native descen-dants, this pattern is statistically significant only forthe generic area analysis (Table 5.3, note: alltables and appendices are available on the websitepalaeo-electronica.org/2010_1/index.html); how-ever, when Strophomena species are treated asinvasive, ranges of invader taxa are significantlysmaller in all analyses except the species linearanalysis. Finally, the geographic ranges of newspecies that evolve in the Richmondian from Cin-cinnatian ancestors are significantly smaller thanthe ranges of carryover taxa in the Richmondian in

all analyses (Table 5.4, note: all tables and appen-dices are available on the website palaeo-electron-ica.org/2010_1/index.html).

Comparison by Sequence

A second way to assess the biogeographicimpact of the Richmondian Invasion is to examinepatterns temporally. Species ranges illustrated inFigure 4 are representative of patterns for eachtime slice. Geographic range size for speciesgroups within each depositional sequence wereassessed through Analysis of Variance (ANOVA)

Carryover

Maysvillian Restricted

Carryover


Carryover


Native Descendant

Carryover

20 6040 8004a Extrabasinal Invader

Native Descendant

Carryover

20 6040 8005a Extrabasinal Invader

Native Descendant

Carryover

20 6040 800

95% CI for Normalized Mean Geographic Range

6a Extrabasinal Invader

Carryover in Maysvillian

Carryover in Richmondian

Extrabasinal Invaders

Native Descendants

20 6040 807a


0

20 6040 8001

20 6040 8002

20 6040 8003

20 6040 8004b

20 6040 8005b

20 6040 8006b

20 6040 807b

0

FIGURE 5. Comparison of the normalized mean species range from the area method for each species group bysequence (1-6 relate to corresponding sequence number) and for the entire study interval (7). 4-7 (a) treat Richmon-dian Strophomena species as native descendants, while (b) treat Richmondian Strophomena species as invasive.Individual 95% confidence intervals for mean geographic range are based on pooled standard deviation.

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tests. Results are similar regardless of normaliza-tion procedure or whether Richmondian occur-rences of Strophomena were coded as native orinvasive in origin (Figure 5, Table 6, Appendices 4,5, 7, 9, note: all tables and appendices are avail-able on the website palaeo-electronica.org/2010_1/index.html). Differences in statistical signif-icance between tests using the different codingstrategies are relatively minor and are restricted tothe C4 and C5 sequences (Table 6, note: all tablesand appendices are available on the websitepalaeo-electronica.org/2010_1/index.html).

In the C1 sequence, there is no statistical dif-ference between geographic ranges of taxa whichwill ultimately survive into the Richmondian andthose that become extinct by the end of theMaysvillian (Figure 5.1, Table 6.1, note: all tablesand appendices are available on the websitepalaeo-electronica.org/2010_1/index.html). In theC2 sequence, Maysvillian restricted taxa occupysmaller geographic ranges than carryover taxa,although this is statistically significant in only half ofthe analyses of the species area method (Figure5.2, Table 6.2, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html). In the C3 sequence, Maysvil-lian restricted taxa occupy geographic ranges thatare statistically smaller than carryover taxa in allanalyses (Figure 5.3, Table 6.3, note: all tables andappendices are available on the website palaeo-electronica.org/2010_1/index.html).

The C4 sequence includes the earliest evi-dence of extrabasinal invaders and represents theinitial phases of the invasion and establishment ofinvasion ecology. In this sequence, invader taxaoccupy restricted geographic ranges with respectto the carryover taxa (Figure 5.4). When Strophom-ena species are coded as native descendants, newspeciation is limited to three species (Tables 1, 3,note: all tables and appendices are available onthe website palaeo-electronica.org/2010_1/index.html), but these species are narrowly distrib-uted (Figure 5.4). If Strophomena species arecoded as invasive, then only one native descen-dant species, Platystrophia clarksvillensis, occursin the sequence, which renders analysis of thattaxon group spurious. Even so, differencesbetween carryover, native descendant, and inva-sive species are statistically significant or nearly soin all analyses (Table 6.4)\, note: all tables andappendices are available on the website palaeo-electronica.org/2010_1/index.html).

In the C5 sequence, the most broadly distrib-uted taxa are still the carryover taxa, but invaders

exhibit larger ranges than they did in the C4sequence (Figure 5.5). Newly evolved species,however, continue to occupy restricted ranges (Fig-ure 5.5). Whereas statistical differences betweenthe three classes remain at the genus level, theoverlap between carryover and invader taxa at thespecies level renders these groups biogeographi-cally indistinguishable (Table 6.5, note: all tablesand appendices are available on the websitepalaeo-electronica.org/2010_1/index.html). By thelate Richmondian C6 sequence, all class size dif-ferentiation has broken down and differences areno longer statistically significant in any analysis(Figure 5.6, Table 6.6, note: all tables and appendi-ces are available on the website palaeo-electron-ica.org/2010_1/index.html).

DISCUSSION

Variations in Geographic Range between Taxon Groups

The patterns of differentiation in the geo-graphic ranges observed in taxonomic groups ofCincinnatian brachiopods can be explained, atleast partly, by the relationship between geo-graphic range size and niche breadth. The geo-graphic range inhabited by a species is amanifestation of a species ecological niche at twolevels, the fundamental and realized niche(Lomolino et al. 2006). The largest geographicrange that a species may potentially occupy is thearea of occurrence of a species’ fundamentalniche, the sum of the ecological parameters underwhich a species is able to maintain a population(Hutchinson 1957). All species, however, actuallyoccupy a smaller geographic region, which isreferred to as the realized niche. The differencebetween a species’ fundamental and realizedniches is determined by biotic interactions such ascompetition and predation (Hutchinson 1957). Spe-cies geographic ranges, therefore, are directly tiedto the breadth of their ecological niche. A positivecorrelation between niche breath and geographicrange has been recovered in numerous studies(e.g., Jackson 1974; Jackson et al. 1985; Brown1984; Thompson et al. 1999; Gaston and Spicer2001; Fernández and Vrba 2005; but see Williamset al. 2006 for a counterexample). Species withbroad environmental tolerances, known as gener-alist or eurytopic species, exhibit larger geographicranges than specialist or stenotopic species, whichare characterized by highly constrained niches(MacArthur 1972; Mayr 1963; Stanley 1979).Because specialists can utilize only a limited array

11


of ecological parameters, the geographic region,which encompasses their niche, will necessarily besmaller than those of eurytopic species.

Based on the relationship between geo-graphic range and niche breadth, the ecologicalcharacteristics of the four brachiopod groups canbe considered. Both Maysvillian restricted taxa andnew species that evolve in the Richmondian fromnative taxa exhibit small range sizes characteristicof ecological specialists (Figures 4, 5.7). Extrabasi-nal invaders are characterized by intermediategeographic ranges, and carryover taxa exhibitlarge geographic ranges suggestive of ecologicalgeneralists (Figures 4, 5.7). Statistical results fur-ther support the classification of the Maysvillianrestricted and native descendant species into onecategory of narrower niche breadth versus the car-ryover and invasive taxa into a second category ofbroader niche breadth. The geographic ranges ofboth the Maysvillian restricted taxa and the nativedescendant species are statistically significantlysmaller than the carryover taxa (Table 5.1, 5.4,note: all tables and appendices are available onthe website palaeo-electronica.org/2010_1/index.html). Conversely, the geographic ranges ofthe invader taxa, although smaller on average thancarryover taxa, are statistically indistinguishablefrom the carryover taxa in several comparisons,particularly those conducted at the species level(Table 5.3, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html, Figure 5.7). This apparent dis-parity between the two generalist groups resultsfrom temporal shifts in the geographic ranges ofthese groups, discussed more fully below.

The assignment of these taxon groups to spe-cialist versus generalist ecologies is also consis-tent with their macroevolutionary histories. Ingeneral, specialist and generalist species exhibitcharacteristic differences in speciation and extinc-tion rates; namely, generalist species tend to belonger lived with lower rates of extinction and spe-ciation (Jackson 1974; Stanley 1979; Foote et al.2008). This macroevolutionary relationship is aderivative of niche breadth; the larger the geo-graphic region occupied by a species, the morelikely that at least some part of that range willremain habitable following events of environmentalor biotic perturbation. Consequently, one wouldpredict a priori that the longest lived species in thedataset, the carryover species, should exhibitlarger geographic ranges indicative of generalistecologies; a prediction congruent with the results.In addition, the two specialist groups, the Maysvil-

lian restricted taxa and the newly evolved descen-dant species, would be predicted to exhibit shortertemporal durations, which is also congruent withthe results. Presumably, the native descendanttaxa radiated into open specialist niches vacatedby the extinction of the Maysvillian restricted spe-cies. Furthermore, the interpretation of invadertaxa as ecological generalists is consistent withdata from the modern invasion biology literature;most of the introduced species that have success-fully invaded new ecosystems exhibit broad eco-logical tolerances (Davis 2009).

The stark difference between the geographicrange size of the species and genera that becomeextinct by the end of the Maysvillian versus therange size of the carryover taxa (Table 5.1, note: alltables and appendices are available on the websitepalaeo-electronica.org/2010_1/index.html)sug-gests that species with limited niche breadth wereunable to succeed in the new invasive regime incontrast to species with broader niches. Becausethe carryover taxa are present both before andafter the influx of the invaders, it is possible thatthese taxa would have experienced a reduction intheir realized niche, and hence geographic range,due to increased biotic interactions with the inter-basinal invaders. To test this hypothesis, the geo-graphic ranges of carryover taxa were comparedbefore and after the onset of the invasion. Althoughmean taxon range decreased slightly after the inva-sion (more noticeably at the species level than thegeneric level), these differences were not statisti-cally significant in any analysis (Table 5.2, note: alltables and appendices are available on the websitepalaeo-electronica.org/2010_1/index.html). Prioranalyses (e.g., Tyler and Leighton 2007) havenoted shifts in morphology of incumbent generawhen they co-occur with morphologically similarinvaders; however, these differences appear torepresent local effects that do not manifest in spe-cies or genus-level geographic patterns.

An alternate explanation for the limited rangesize of invader and native descendant speciesrelates to the relationship between geographicrange size and taxon age. All taxa necessarilyoccupy small geographic ranges immediately fol-lowing speciation, expand their geographic rangesas population sizes increase through time, andcontract their geographic ranges as population sizedecreases prior to extinction (Vrba and DeGusta2004; Foote et al. 2008). Consequently, youngspecies may be expected to occupy smaller geo-graphic ranges than older species with large popu-lation sizes (Webb and Gaston 2000). Studies of

12


the timing of range expansion in the fossil recordhave determined that geographic range sizeincreases rapidly following speciation (Liow andStenseth 2007), and species typically attain fullrange size within one million years or less (Vrbaand DeGusta 2004; Webb and Gaston 2000).Since the scale of temporal resolution of this studyis approximately one million years per time slice, itis unlikely that the estimates of geographic rangesize analyzed herein capture the early post-specia-tion phase prior to full range size establishment.This possibility, however, cannot be excluded com-pletely and may contribute to the observedincrease in average geographic range of nativedescendant species from the C4 to C6 sequenceor invader species between the C4 and C5sequences.

Temporal Variations in Geographic Range

Biogeographic patterns shift dramaticallyacross the six Cincinnatian sequences (e.g., Figure5). From C1 to C3 sequences, carryover taxaexhibit larger mean geographic range size thanMaysvillian restricted taxa. However, this differenceis statistically significant only during the C3sequence (Table 6, note: all tables and appendicesare available on the website palaeo-electron-ica.org/2010_1/index.html). Apparently, it is duringthe final Maysvillian sequence only when establish-ing a larger geographic range is a predictor fortaxon success across the invasion interval. At theonset of the Richmondian Invasion in the C4sequence, carryover taxa are characterized bylarge mean geographic range sizes, and both newdescendant species and invader taxa exhibitsmaller ranges than carryover taxa (significant inthree of four analyses for either coding scheme).New speciation is limited to only one to three spe-cies, but these are narrowly distributed, specialiststyle species. By the C5 sequence, a very diverseset of taxa is present. The most broadly distributedtaxa are still the carryover taxa, but invadersexhibit larger ranges than their C4 sequence coun-terparts. Newly evolved species continue to occupyrestricted ranges characteristic of ecological spe-cialists. Although statistical differences remain atthe genus level, the overlap between carryover andinvader taxa at the species level renders thesegroups biogeographically indistinguishable in theC5 sequence. Finally, during the C6 sequenceclass differentiation breaks down and carryover,new species, and invader taxa have overlappingmean geographic ranges.

Holland and Patzkowsky (2007) interpretedthree phases of community organization from theirgeneric-level analysis of paleocommunity struc-ture: stability from C1 to C3, reorganization in C4,and stability in C5 and C6 sequences. Our resultsare largely congruent with their pattern. Similar bio-geographic patterns appear in C1 through C3sequences, but each of C4, C5, and C6 exhibit dif-ferent organizational patterns (Table 6, note: alltables and appendices are available on the websitepalaeo-electronica.org/2010_1/index.html, Figure5).

The observed shifts in Richmondian biogeo-graphic ranges, particularly the increase in invaderrange between the C4 and C5 sequence and thereduction in range size of both carryover andinvader taxa between the C5 and C6 sequences,could potentially be attributed to several causes:response to invasive regime, niche shift of speciesdue to environmental rather than biotic changes, orsampling bias. In this case, sampling bias can beruled out as a primary driver of the observed pat-tern. The C4 sequence comprises only two of thefour Cincinnatian depositional environments (deepand shallow subtidal), whereas the C5 sequenceincludes deposits of all four environments (alsoincluding offshore and peritidal) (Brett and Algeo2001; Holland 2001). Based on ordination analy-ses, invader taxa most commonly occur in thedeep and shallow subtidal communities, which arepreserved in both the C4 and C5 sequences (Hol-land and Patzkowsky 2007). Because the percentarea colonized by invaders increases with addi-tional facies, range increase observed in the C5sequence cannot be attributed to undersampling offacies. Furthermore, biogeographic patterns recov-ered when geographic range is normalized bynumber of localities (a proxy for sampling intensity)are congruent with those recovered from the out-crop area normalization method (compare Table 6and Appendix 4, note: all tables and appendicesare available on the website palaeo-electron-ica.org/2010_1/index.html). This finding indicatesthat observed biogeographic patterns are not con-trolled by sampling bias. The C6 sequence exhibitspotential for sampling bias as this sequence is bothgeographically restricted (Figure 1) and limited toonly the shallow subtidal and peritidal facies (Hay2001), and this limitation should be consideredwhen interpreting C6 patterns. Paleoenvironmentalchanges can be ruled out on similar grounds. Allsequences record shallowing upward (Holland1993); symmetrical biogeographic patterns, there-fore, should be expected between sequences if

13


range sizes are strongly affected by changes in rel-ative sea level. Aside from the oceanographic shiftin the early Richmondian—which affected all sub-sequent sequences equally, no significant paleoen-vironmental changes are recordedsedimentologically. The biotic impact of the extra-basinal invaders, therefore, emerges as the mostlikely cause of the observed biogeographic shift.

Characteristics of Richmondian Invaders

A significant body of research has emergedwithin the modern invasion biology literature aimedat delimiting the characteristics of species that suc-cessfully invade new ecosystems (see review inDavis 2009). For a species to successfully invade anew habitat, four basic stages must occur: trans-port, establishment, spread, and impact (Lockwoodet al. 2007). Modern invasive species must exhibittraits that facilitate both the transport and establish-ment stages. Certain characteristics, such asaccess to human transport devices (ship ballastwater, fruit cargo containers) are matters of contin-gency; whereas other characteristics, such as theability to exploit a variety food sources in the newecosystem relate directly to the biological parame-ters of a species.

The most important feature for determiningspecies’ success during the transport stage ispropagule pressure, both the number of individualsarriving at a location and the frequency of theirintroduction (Lockwood et al. 2005). In the fossilrecord, transport occurs through natural, in thiscase oceanographic, processes. In the Richmon-dian, successful invaders would have exhibitedhigh larval or adult dispersal in order to establishnew populations at such large distances from theirancestral populations. Richmondian propagulepressure was likely much lower than that observedwith invaders in modern ecosystems as tens ofthousands of years were available for transportand establishment of the Late Ordovician taxa.

Establishment relates to initial colonization ofthe new habitat by a small number of individuals,whereas spread refers to the stage in which theinvader species is both abundant and becomingwidespread. Species with broad ecological toler-ances are more likely to succeed in these stagesthan ecological specialists (Duncan et al. 2003;Lockwood et al. 2007). Due to the short durationand small population sizes during this interval,these stages are unlikely to be preserved in thefossil record. Instead, the first appearance of Rich-mondian Invaders in the fossil record most likelyreflects the impact stage, which refers to the inter-

val when the invader taxon is fully established andnaturalized or integrated within the community(Lockwood et al., 2007).

Within the rhynchonelliform brachiopods, theRichmondian invaders appear to conform to thebasic set of expectations developed from moderninvasion biology: high dispersal ability and broadecological tolerances. Although adult rhynchonelli-form brachiopods lack locomotor ability, their lar-vae are free swimming. The duration of the free-swimming larval stage may persist several weeks(Rudwick 1970, Peck and Robinson 1994), andrecent rhynchonelliform brachiopod species havebeen observed to expand their ranges as much as3000 to 4000 km in only 10,000 years (Curry andEndo 1991). If Ordovician brachiopods exhibitedsimilar larval development, then propagule pres-sure would be sufficiently high in these species toproduce the observed interbasinal invasions rap-idly once the oceanographic patterns shifted in theearly Richmondian Age. Furthermore, the geo-graphic ranges of the invader species statisticallyoverlap those of the generalist carryover species(Table 5.3, note: all tables and appendices areavailable on the website palaeo-electronica.org/2010_1/index.html). The Richmondian invaders,therefore, also exhibit the large geographic rangescharacteristic of broadly adapted species.

Although the geographic ranges of invadertaxa are statistically similar to the carryover taxa atthe species level, differences emerge at the genuslevel (Table 5.3, note: all tables and appendicesare available on the website palaeo-electron-ica.org/2010_1/index.html). This pattern is partlyattributable to the fact that most invasive generaare monotypic within the Cincinnati region whereassome native genera include multiple species. Sincethe monophyly of these genera is also question-able, the species-level comparison may be a morerobust comparison of carryover versus invasivetaxa across the aggregated sequences. However,the sequence level details also suggest a morecomplex pattern than the species level aggregateanalysis. In the C4 sequence, geographic range forinvader taxa is significantly smaller (in all variationsof analyses) than in the C5 sequence. This appar-ent shift in range size may be a sampling artifact.There are only three (or five) C4 invaders versus12 (or 17) C5 invaders, and two of the three spe-cies exhibit C4 range sizes close to their C5 rangesize. Even so, the observed lag in either rangeestablishment or expansion of range size amongthe invaders potentially indicates that the full bioticimpact of the invasion was spread across the C4

14


and into the C5 sequences, an interval of at leastone million years.

Impact of the Richmondian Invaders

The recovered biogeographic patterns sug-gest that during the early stages of the biotic inva-sion, in the transition from the C3 to the C4sequence, narrowly adapted native species did notadjust to the invasive regime and become extinct,while broadly adapted native species persisted andflourished. The native generalists, in fact, appear tobe more successful at establishing broad geo-graphic ranges than the newly invading taxa in thefirst two million years after the initial invasion.Meanwhile, new species that evolved in the Rich-mondian from Cincinnati natives occupied smallergeographic ranges than either the carryover orinvader taxa in both the C4 and C5 sequences(Figure 5, Table 6, note: all tables and appendicesare available on the website palaeo-electron-ica.org/2010_1/index.html). The mean range sizeof the new species overlaps with the range sizevacated by the Maysvillian restricted species; thissuggests that species evolving after the initial C4reorganization radiated into open specialist niches.Speciation is very limited in the C4 sequence,which may be due to the introduction of invaders. Apattern of reduced speciation rate associated withintervals of high interbasinal invasion has alsobeen reported for Late Devonian brachiopods (Sti-gall 2008, 2010).

As noted by Patzkowsky and Holland (2007),the overall effect of the introduction of the invadertaxa was to increase local diversity. Studies ofmodern coastal ecosystems have also docu-mented increases rather than decreases in totaldiversity following the introduction of invasive spe-cies (Reise et al. 2006). Although ecologically spe-cialized Maysvillian species become extinct by theend of the C3 sequence as discussed above, thisdid not result in an abrupt extinction peak becausethese extinctions are spread out over twosequences (Table 1, note: all tables and appendi-ces are available on the website palaeo-electron-ica.org/2010_1/index.html; Holland 1997). Inmodern marine ecosystems, no compelling evi-dence exists for species extinction caused by com-petition with invasive species (Davis 2003). Basedon the results of the Cincinnatian analysis, itappears that the long-term impacts of species inva-sions, at least in the case of the Richmondian Inva-sion, also do not result in extinction from directcompetition for resources between native and inva-sive taxa. In fact, based on biogeographic data, it

appears that the influx of invaders had no impacton reducing the realized niche of native carryovertaxa. Instead, invasive species were limited byincumbent taxa to smaller realized niches duringthe C4 sequence compared with their C5 niches.This suggests that native communities, at least thegeneralist taxa within these communities, are moreresilient to invader domination that suggested byshort-term ecological observations.

CONCLUSIONS

By analyzing the geographic ranges of Cincin-natian rhynchonelliform brachiopod species in atemporal framework, a clear picture of the biogeo-graphic impact of the Richmondian invaders beginsto emerge. Native Cincinnatian species with smallgeographic ranges in the Maysvillian do not crossinto the Richmondian, whereas species thatoccupy large geographic ranges do. In fact, nativetaxa that carryover into the Richmondian havelarger geographic ranges than the invader taxauntil the C5 sequence—at least one million yearsafter the invasion. Evidently narrowly adapted, eco-logical specialists were more significantly impactedby ecosystem change associated with the invasiveregime than ecological generalists. Conversely,native generalist taxa continue to occupy largegeographic ranges with no discernable contractionof range size following the influx of the invaders.The invader taxa exhibit statistically smaller rangesizes than native carryover taxa initially, suggestingthat native communities were somewhat resilient toinvader domination. Speciation rate is low in the C4sequence during the establishment of the invasiveregime, but increases in the C5 sequence. Newspecies that evolve in the Richmondian from Cin-cinnati natives occupy smaller geographic rangesthan either the carryover or invader taxa in both theC4 and C5 sequences. The range size of thesenew taxa overlaps with the range size vacated bythe ecological specialists of the Maysvillian Stage.In the C6 sequence, the differentiation betweeninvader and native taxa appears to break down.

The long-term effects of invasive species ofthe Richmondian Invasion can be summarized asfollows. Geographically restricted stenotopic spe-cies are the most susceptible to extinction duringthe invasive regime. Inferred competition betweeninvader taxa and native eurytopic taxa does notresult in either reduction in geographic range sizeor realized niches of native taxa. Speciation maybe reduced during invader establishment, and newspecies that evolve following invader establish-ment are ecological specialists. Results also indi-

15


cate that overall, the ecological effects of theRichmondian Invasion were long lasting—throughboth the C4 and C5 sequences. The protractedbiogeographic response to invasion agrees withresults of biofacies analyses by Holland and Patz-kowsky (2007) in general, although this analysissuggests that a stable ecosystem may not have re-established until the C6 sequence.

Invasive species pose a significant problemfor modern ecosystems. Invasion biologists havedocumented clear patterns of increased competi-tion, predation, and ecosystem restructuring in theyears and decades following invasion events(Lockwood et al. 2007) but lack the temporal datato determine how these short-term patterns mayscale up over long time spans. Analyses, such asthis one, can provide insight into the ultimate resultof these short term impacts. The biogeographicresponse of native Cincinnatian taxa to the Rich-mondian invasion indicates that ecological special-ists are most vulnerable to extirpation duringinvasive regimes, but competition between nativegeneralists and invasive species does not result inextinction of either native or invasive species.Rather, total ecosystem diversity is enhanced.Although stenotopic species become extinct at theonset of the ecosystem reorganization, they arelater replaced by newly evolved species character-ized by similar niche breadth. New speciation,however, appears to be retarded during the initialwaves of the invasion. Moreover, the results of thisanalysis indicate that invasion effects are likely tobe long lasting. These results indicate that earlyintervention of new exotic introductions and protec-tion of native ecological specialists in environmentsthat are already impacted by invasion should beconservation priorities in modern ecosystems.

ACKNOWLEDGMENTS

Thanks to C. Stock and L. Leighton for con-structive reviews that improved an earlier versionof this paper. B. Klingensmith assisted with datacollection, and Jacqueline Smith assisted withpolygon creation. D. Gneidovic (Ohio State OrtonGeological Museum), K. Hauer (Miami UniversityLimper Museum), and B. Hunda (CincinnatiMuseum of Natural History) are thanked for accessto and assistance with their collections. Thisresearch was supported by NSF EAR- 0922067, agrant from the American Chemical Society’s Petro-leum Research Fund, Ohio University Baker Fundand PACE Awards, and the Ohio UniversityDepartment of Geological Sciences.

REFERENCES

Anstey, R.L., Rabbio, S.F., and Tuckey, M.E. 1987. Bryo-zoan bathymetric gradients within a Late Ordovicianepeiric sea. Paleoceanography, 2:165-176.

Barbour, S.L. 2001. Multi-scale analysis of spatial faunalvariability and microstratigraphy in the Fairview For-mation (Upper Ordovician), Northern Kentucky, p.117-122. In Algeo, T.J. and Brett, C.E. (eds.),Sequence, Cycle, and Event Stratigraphy of UpperOrdovician and Silurian Strata of the Cincinnati ArchRegion. Kentucky Geological Survey, Field TripGuidebook, 1 (Series 12).

Brandt-Velbel, D. 1985. Ichnologic, taphonomic, nd sedi-mentologic clues to the deposition of Cincinnatianshales (Upper Ordovician), Ohio, USA, p. 299-307. InCurran, H.A. (ed.), Biogenic Structures: Their Use inInterpreting Depositional Environments. SEPM Spe-cial Publication 35.

Brett, C.E. and Algeo, T.J. 2001. Sequence Stratigraphyof Upper Ordovician and Lower Silurian Strata of theCincinnati Arch Region, p. 34-46. In Algeo, T.J. andBrett, C.E. (eds.), Sequence, cycle, & event stratigra-phy of upper Ordovician & Silurian strata of the Cin-cinnati Arch region. Kentucky Geological Survey,Field Trip Guidebook, Series 12, Guidebook 1.

Brown, J.H. 1984. On the relationship between abun-dance and distribution of species. The American Nat-uralist, 124:255-279.

Curry, G.B. and Endo, K. 1991. Migration of brachiopodspecies in the North Atlantic in response to Holoceneclimatic change. Geology, 19:1101-1103.

Dattilo, B.F. 2004. A new angle on strophomenid paleo-ecology: trace-fossil evidence of an escape responsefor the plectambonitoid brachiopod Sowerbyellarugosa from a tempestite in the Upper OrdovicianKope Formation (Edenian) of Northern Kentucky.Palaios, 19: 332-348.

Davis, M.A. 2003. Biotic globalization: does competitionfrom introduced species threaten biodiversity? Bio-science, 53:481-489.

Davis, M.A. 2009. Invasion Biology. Oxford UniversityPress, Oxford.

Davis, R.A. 1998. Cincinnati Fossils: An ElementaryGuide to the Ordovician Rocks and Fossils of theCincinnati, Ohio Region. Cincinnati Museum of Natu-ral History, Cincinnati, Ohio.

Davis, R.A. and Cuffey, R.J. 1998. Sampling the LayerCake That Isn't: The Stratigraphy and Paleontologyof the Type-Cincinnatian. Ohio Division of GeologicalSurvey, Guidebook, 13:1-194.

Duncan, R.P., Blackburn, T.M., and Sol, D. 2003. Theecology of bird introductions. Annual Review of Ecol-ogy and Systematics, 34:71-98.

Elias, R.J. 1983. Middle and Late Ordovician solitaryrugose corals of the Cincinnati Arch region. UnitedStates Geological Survey Professional Paper, 1066-N:N1-N13, 2 pls.

Environmental Systems Research Institute, Inc. (ESRI)2008. ArcGIS 9.3. Redlands, California.

16


Feldmann, R.M. 1996. Fossils of Ohio. Ohio Division ofGeological Survey Bulletin, 70:1-577.

Fernández, M.H. and Vrba, E.S. 2005. Body size, biomicspecialization and range size of large African mam-mals. Journal of Biogeography, 32:1243-1256.

Finnegan, S. and Droser, M.L. 2008. Reworking diver-sity: effects of storm deposition on evenness andsampled richness, Ordovician of the basin and range,Utah and Nevada, USA. Palaios, 23:87-96.

Foerste, A.F. 1917. Notes on Richmond and related fos-sils. Journal of the Cincinnati Society of Natural His-tory, 22:42-55.

Foote, M., Crampton, J. S., Beu, A.G., and Cooper, R.A.2008. On the bidirectional relationship between geo-graphic range and taxonomic duration. Paleobiology,34:421-433.

Frey, R.C. 1987. The occurrence of pelecypods in earlyPaleozoic epeiric sea environments, Late Ordovicianof Cincinnati, Ohio area. Palaios, 2:3-23.

Fritts, T.H. and Rodda, G.H. 1998. The role of introducedspecies in the degradation of an island ecosystem: acase history of Guam. Annual Review of Ecology andSystematics, 29:113-140.

Gaston, K.J. and Spicer, J.I. 2001. The relationshipbetween range size and niche breadth: a test usingfive species of Gammarus (Amphipoda). Global Ecol-ogy and Biogeography, 10:179-188.

Hay, H.B. 2001. Paleogeography and paleoenviron-ments, Fairview through Whitewater Formations(Upper Ordovician, southeastern Indiana and south-western Ohio), p. 120-134. In Algeo, T.J. and Brett,C.E. (eds.), Sequence, Cycle, and Event Stratigraphyof Upper Ordovician and Silurian Strata of the Cincin-nati Arch Region. Kentucky Geological Survey, FieldTrip Guidebook, 1 (Series 12).

Hendricks, J.R., Lieberman, B.S., and Stigall, A.L. 2008.Using GIS to study the paleobiogeographic and mac-roevolutionary patterns in soft-bodied Cambrianarthropods. Palaeogeography, Palaeoclimatology,Palaeoecology, 264:163-175.

Holland, S.M. 1993. Sequence stratigraphy of a carbon-ate-clastic ramp: the Cincinnatian Series (UpperOrdovician) in its type area. Geological Society ofAmerica Bulletin, 105:306-322.

Holland, S.M. 1997. Using time/environment analysis torecognize faunal events in the Upper Ordovician ofthe Cincinnati Arch, p. 309-334. In Brett, C.E. andBaird, G.C. (eds.), Paleontological Events: Strati-graphic, Ecological, and Evolutionary Implications.Columbia University Press, New York.

Holland, S.M. 2001. Sequence stratigraphy of the Cin-cinnatian Series (Upper Ordovician, Cincinnati, OhioRegion), p. 135-151. In Algeo, T.J. and Brett, C.E.(eds.), Sequence, Cycle, and Event Stratigraphy ofUpper Ordovician and Silurian Strata of the Cincin-nati Arch Region. Kentucky Geological Survey, FieldTrip Guidebook, 1 (Series 12).

Holland, S.M. 2005. The signatures of patches and gra-dients in ecological ordinations. Palaios, 20:573-580.

Holland, S.M. 2008. The type Cincinnatian: An overview,p. 174-184. In McLaughlin, P.I. Brett, C.E., Holland,S.M. and Storrs, G.W. (eds.), Stratigraphic Renais-sance in the Cincinnati Arch: Implications for UpperOrdovician Paleontology and Paleoecology. Cincin-nati Museum Center Scientific Contributions 2, Cin-cinnati, Ohio.

Holland, S.M. and Patzkowsky, M.E. 1996. Sequencestratigraphy and long-term paleoceanographicchange in the Middle to Upper Ordovician of the east-ern United States, p. 117-130. In Witzke, B., Day, J.and Ludvigson, G.A. (eds.), Paleozoic SequenceStratigraphy: Views from the North American Craton.Geological Society of America, Special Paper, 306.Boulder, Colorado.

Holland, S.M. and Patzkowsky, M.E. 2007. Gradientecology of a biotic invasion: Biofacies of the type Cin-cinnatian Series (Upper Ordovician), Cincinnati, OhioRegion, USA. Palaios, 22:392-407.

Holland, S.M. and Patzkowsky, M.E. 2009. The strati-graphic distribution of fossils in a tropical carbonatesucession: Ordovician Bighorn Dolomite. Palaios,24:303-317.

Holland, S.M., Miller, A.I., Meyer, D.L., and Datillo, B.F.2001. The detection and importance of subtle biofa-cies within a single lithofacies: The Upper OrdovicianKope Formation of the Cincinnati, Ohio region.Palaios, 16:205-217.

Hutchinson, G.E. 1957. Concluding remarks. Cold SpringHarbor Symposium on Quaternary Biology, 22:415-427.

Jackson, J.B.C. 1974. Biogeographic consequences ofeurytopy and stenotyopy among marine bivalves andtheir evolutionary significance. The American Natu-ralist, 108:541-560.

Jackson, J.B.C., Winston, J.E., and Coastes, A.G. 1985.Niche breadth, geographic range, and extinction ofCaribbean reef-associated cheilostome Bryozoa andScleractinia. Proceedings of the Fifth InternationalCoral Reef Congress, Tahiti, 4:151-168.

Jennette, D.C. and Pryor, W.A. 1993. Cyclic alternationof proximal storm facies: Kope and Fairview forma-tions (Upper Ordovician), Ohio and Kentucky. Jour-nal of Sedimentary Petrology, 63:183-203.

Jin, J. and Zhan,R.-B. 2001. Late Ordovician articulatebrachiopods from the Red River and Stony MountainFormations, Southern Manitoba. NRC ResearchPress, Ottawa, Ontario, Canada.

Kidwell, S.M. and Flessa, K.W. 1996. The quality of thefossil record: populations, species, and communities.Annual Review of Earth and Planetary Science,24:433-464.

Leighton, L.R. 1998. Constraining functional hypotheses;controls on the morphology of the concavo-convexbrachiopod Rafinesquina. Lethaia, 31:293-307.

Liow, L.H. and Stenseth, N.C. 2007. The rise and fall ofspecies: implications for macroevolutionary and mac-roecological studies. Proceedings of the Royal Soci-ety of London, B, 274:2745-2752.

17


Lockwood, J.L., Cassey, P., and Blackburn, T.M. 2005.The role of propagule pressure in explaining speciesinvasions. Trends in Ecology and Evolution, 20:223-228.

Lockwood, J., Hoopes, M., and Marchetti, M. 2007. Inva-sion Ecology. Blackwell Publishing, Singapore.

Lomolino, M.V., Riddle, B.R., and Brown, J.H. 2006. Bio-geography, third edition. Sinauer Publishers, Sunder-land, Massachusetts.

MacArthur, R.H. 1972. Geographical Ecology: Patternsin the distribution of species. Harper and Row, NewYork.

Mayr, E. 1963. Animal Species and Evolution. Belknap,Cambridge.

Meyer, D.L. 1990. Population paleoecology and compar-ative taphonomy of two edrioasteroid (Echinoder-mata) pavements: Upper Ordovician of Kentucky andOhio. Historical Biology, 4,155-178.

Meyer, D.L. and Davis, R.A. 2009. A Sea Without Fish:Life in the Ordovician Sea of the Cincinnati Region.Indiana University Press, Bloomington, 346 p.

Miller, A.I., Holland, S.M., Meyer, D.L., and Datillo, B.F.2001. The use of faunal gradient analysis for intrare-gional correlation and assessment of changes in sea-floor topography in the Type Cincinnatian. Journal ofGeology, 109:603-13.

Minitab Inc. 2007. Minitab Release 15. State College,Pennsylvania.

Novak-Gottshall , P.E. and Miller, A.I. 2003. Comparativetaxonomic richness and abundance of Late Ordovi-cian gastropods and bilvales in mollusc-rich strata ofthe Cincinnati Arch. Palaios, 18:559-571.

Patzkowsky, M.E. and Holland, S.M. 1996. Extinction,invasion, and sequence stratigraphy; Patterns of fau-nal change in the Middle and Upper Ordovician of theEastern United States, p. 131-142. In Witzke, B.,Day, J., and Ludvigson, G.A. (eds.), PaleozoicSequence Stratigraphy: Views from the North Ameri-can Craton. Geological Society of America, SpecialPaper, 306. Boulder, Colorado.

Patzkowsky, M.E. and Holland, S.M. 2007. Diversity par-titioning of a Late Ordovician biotic invasion: Controlson diversity in regional ecosystems. Paleobiology,33:295-309.

Peck, L.S. and Robinson, K. 1994. Pelagic larval devel-opment in the brooding Antarctic brachiopod Liothy-rella uva. Marine Biology, 120:279-286.

Reise, K., Olenin, S., and Thieltges, D.W. 2006. Arealiens threatening aquatic coastal ecosystems? Hel-goland Marine Research, 60:77-83.

Rode, A.L. and Lieberman, B.S. 2004. Using GIS tounlock the interactions between biogeography, envi-ronment, and evolution in Middle and Late Devonianbrachiopods and bivalves. Palaeogeography, Palae-oclimatology, Palaeogeography, 211:345-359.

Rode, A.L. and Lieberman, B.S. 2005. Integrating bioge-ography and evolution using phylogenetics andPaleoGIS: A case study involving Devonian crusta-ceans. Journal of Paleontology, 79:267-276.

Rudwick, M.J.S. 1970. Fossil and Living Brachiopods.Hutchinson, London.

Scotese, C.R. and McKerrow, W.S. 1991. Ordovicianplate reconstructions, p. 271-282. In Barnes, C.R.and Williams, S.H. (eds.), Advances in Ordoviciangeology. Canadian Geological Survey, Paper 90-9.

Stanley, S.M. 1979. Macroevolution: Pattern and Pro-cess. W.H. Freeman & Co., San Francisco.

Stigall, A.L. 2006. Getting Started with GIS for Paleobio-geographic Reconstruction: Using Excel, PaleoGIS,Point Tracker, ArcView 3.x, and ArcGIS 9.x. Elec-tronic book, http://oak.cats.ohiou.edu/~stigall/PDFs/GISreconstructionguide.pdf/.

Stigall, A.L. 2008. Tracking species in space and time:Assessing the relationships between paleobiogeog-raphy, paleoecology, and macroevolution, p. 227-242. In Kelly, P.H. and Bambach, R.K. (eds.), FromEvolution to Geobiology: Research Questions DrivingPaleontology at the Start of a New Century. ThePaleontological Society Papers, volume 14.

Stigall, A.L. 2010. Integrating GIS and phylogenetic bio-geography to assess species-level biogeographicpatterns: A case study of Late Devonian faunaldynamics. In Upchurch, P., McGowan, A., and Slater,C. (eds.), Palaeogeography and Palaeobiogeogra-phy: Biodiversity in Space and Time. CRC Press,Publication date: September 2010.

Stigall Rode, A.L. 2005. The application of GeographicInformation Systems to paleobiogeography: Implica-tions for the study of invasions and mass extinctions,p. 77-88. In Lieberman, B.S. and Stigall Rode, A.L.(eds.), Paleobiogeography: Generating New Insightsinto the Coevolution of the Earth and Its Biota. ThePaleontological Society Papers, volume 11.

Stigall Rode, A.L. and Lieberman, B.S. 2005. Using envi-ronmental niche modeling to study the Late Devonianbiodiversity crisis, p. 93-180 In Over, D.J., Morrow,J.R., and Wignall, P.B. (eds.), Understanding LateDevonian and Permian-Triassic Biotic and ClimaticEvents: Towards an Integrated Approach. Develop-ments in Palaeontology and Stratigraphy, Elsevier,Amsterdam.

Thompson, K., Gaston, K.J., and Band, S.R., 1999.Range size, dispersal and niche breadth in the her-baceous flora of central England. Journal of Ecology,87:150-155.

Tyler, C.L. and Leighton, L.R. 2007. A morphometricapproach to analyzing competition and invasiondynamics in Ordovician brachiopods. GeologicalSociety of America Abstracts with Programs,39(6):531.

Vermeij, G.J. 2005. Invasion as expectation: a historicalfact of life, pp. 315-339. In Sax, D.F., Stachowicz,J.J., and Gaines, S.D. (eds.), Species Invasions:Insights into Ecology, Evolution, and Biogeography.Sinauer Associates, Inc., Sunderland, Massachu-setts.

18


Vrba, E.S. and DeGusta, D. 2004. Do species popula-tions really start small? New perspectives from theLate Neogene fossil record of African animals. Pro-ceedings of the Royal Society of London, B, 359:285-293.

Walker, L.G. 1982. The brachiopod genera Hebertella,Dalmanella, and Heterorthina from the Ordovician ofKentucky. United States Geological Survey Profes-sional Paper, 1066-M:M1-M17, 5 pls.

Webb, T.J. and Gaston, K.J. 2000. Geographic rangesize and evolutionary age in birds. Proceedings ofthe Royal Society of London, B, 267:1843-1850.

Webber, A.J. and Hunda, B.R. 2007. Quantitatively com-paring morphological trends to environment in thefossil record (Cincinnatian Series, Upper Ordovician).Evolution, 61:1455-1465.

Williams, Y.M., Williams, S.E., Alford, R.A., Waycott, M.,and Johnson, C.N. 2006. Niche breadth and geo-graphical range: ecological compensation for geo-graphical rarity in rainforest frogs. Biology Letters,2:532-535.

Zuykov, M.A. and Harper, D.A.T. 2007. Platystrophia(Orthida) and new related Ordovician and Early Silu-rian brachiopod genera. Estonian Journal of EarthSciences, 56:11-34.

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