Body size, energetics, and the Ordovician restructuring of ... · mixed carbonate-clastic depositional envi-ronments. 2. High stratigraphic resolution (single bed or small group of

� 2008 The Paleontological Society. All rights reserved. 0094-8373/08/3403-0003/$1.00

Paleobiology, 34(3), 2008, pp. 342–359

Body size, energetics, and the Ordovician restructuring ofmarine ecosystems

Seth Finnegan and Mary L. Droser

Abstract.—Major shifts in ecological dominance are one of the most conspicuous but poorly un-derstood features of the fossil record. Here we examine one of the most prominent such shifts, theOrdovician shift from trilobite to brachiopod dominance of benthic ecosystems. Using an inte-grated database of high-resolution paleoecological samples and body size data, we show that whilethe average local richness and relative abundance of trilobites declined significantly through theOrdovician, the estimated standing biomass of trilobites, and by implication the amount of energythat they used, remained relatively invariant. This is attributable to an increase in the average bodysize of trilobite species in our data set, and especially to the widespread occurrence of the excep-tionally large Middle–Late Ordovician trilobite genus Isotelus. Brachiopods increase in both meanbody size and relative abundance throughout the Ordovician, so that estimates of brachiopod bio-mass and energetic use increase substantially between the Early and Late Ordovician. Althoughthe data set includes a range of depositional environments, similar trends are observed in bothshallow subtidal and deep subtidal settings. These results suggest that diversification of the Pa-leozoic Fauna did not come at the energetic expense of the Cambrian Fauna. The declining relativeabundance of trilobites may reflect a combination of numerical dilution and the necessary energetictrade-offs between body size and abundance.

Seth Finnegan. Department of Geological and Environmental Sciences, Stanford University, 450 SerraMall, Building 320, Stanford, California 94305. E-mail: [email protected]

Mary L. Droser. Department of Earth Sciences, University of California, Riverside, California 92521.

Accepted: 1 April 2008

Introduction

One of the most remarkable episodes of bio-diversification in Earth history took place dur-ing the Ordovician Period (490–443 Ma). Nu-merous clades experienced major evolution-ary radiations during this interval, increasingglobal diversity of marine genera by morethan 300% (Sepkoski 2002). These radiationsdramatically changed the structure of marineecosystems as benthic paleocommunitiesdominated by trilobites and other members ofthe Cambrian Evolutionary Fauna (EF) gaveway to paleocommunities dominated by rhyn-chonelliform (articulate) brachiopods and oth-er members of the Paleozoic EF (Sepkoski andSheehan 1983; Sepkoski and Miller 1985; Pe-ters 2004), establishing an ecological regimethat persisted broadly for the remainder of thePaleozoic Era.

The nature of this restructuring is contro-versial. Although it is clear that the relativespecies richness and abundance of trilobites,the principal members of the Cambrian EF, de-clined in nearshore and midshelf environ-ments, it is not clear whether this indicates

true decline in their ecological significance oris simply due to passive numerical dilution bythe expanding Paleozoic EF (Westrop and Ad-rain 1998a,b; Westrop et al. 1995). The ecolog-ical implications of these two interpretationsare quite distinct. The first implies either thatthere were competitive interactions, direct ordiffuse, between the Cambrian and PaleozoicEFs (Sepkoski and Miller 1985; Sepkoski andSheehan 1983), or that the shift in dominancereflects physical transitions in benthic envi-ronments that favored the Paleozoic EF overthe Cambrian EF (e.g., Miller and Connolly2001). The second scenario instead impliesthat the Paleozoic EF diversified and becametaxonomically dominant by radiating intocomparatively open ecospace (Valentine1973), taking advantage of resources that wereunderutilized by the Cambrian EF (Bambach1983, 1985).

This distinction between actively and pas-sively driven shifts in dominance lies at theheart of many questions about major ecologi-cal transitions in the fossil record (Gould andCalloway 1980; Benton 1996, 1997; Sepkoski

343ORDOVICIAN PALEOCOMMUNITY ENERGETICS

1996; Miller 1998; Sepkoski and Miller 1998;Vermeij 2004). Competitive interactions,whether direct or indirect, are fundamentallyabout the distribution of energy and nutrients,but shifts in dominance have usually been ex-amined using global-scale species or genusrichness data. This approach has been criti-cized both because it is unclear how short-term, local ecological interactions scale up togenerate global macroevolutionary patterns(Dietl and Vermeij 2006), and because it im-plicitly assumes that all species are ecologi-cally equivalent when it is clear from study ofmodern ecosystems (Brown 1995; Kerr andDickie 2001) that this is never true.

In recognition of these limitations, recentanalyses have begun to incorporate abun-dance data as well (Wing et al. 1993; Lupia etal. 1999; Sepkoski et al. 2000; Novack-Gottsh-all and Miller 2003; Peters 2004, 2006; Finne-gan and Droser 2005; Bush et al. 2007). How-ever, abundance by itself is an incompletemeasure of ecological significance, if ecologi-cal significance is understood to have a spe-cifically energetic connotation (Bambach 1993;Vermeij 2004). Another critical factor, which israrely considered in paleoecological studies,is body size.

Because mass and per-individual metabolicrate increase with body size, while populationdensity tends to decrease with body size,standing biomass (average body mass · abun-dance · area�1 · time�1) and population ener-getic use (energy ·area�1 · time�1) are not pre-dictable on the basis of abundance alone (Da-muth 1981, 1987a; Blackburn and Gaston1997). This relationship, termed the EnergeticEquivalence Rule (Damuth 1981) invalidatesabundance as a metric of biomass or energyuse when, as is normally the case, the speciesunder consideration span a wide range ofbody sizes. It also makes the prediction that,all else being equal, increases in mean bodysize, often observed in the fossil record,should be accompanied by decreases in abun-dance. Hence, understanding the ecologicalcontext of major faunal transitions in the fossilrecord requires integrating abundance andbody size data.

Here we combine a database of high-reso-lution paleoecological samples with a data-

base of trilobite and rhynchonelliform bra-chiopod body sizes to estimate Ordoviciantrends in biomass and energy use for thesetwo ecologically and taxonomically importantgroups. We show that due to substantial in-creases in the average body size of both tri-lobites and brachiopods in our data set be-tween the Early and the Late Ordovician,these trends differ significantly from trends ingenus richness and relative abundance, andhave markedly different implications for thenature of ecosystem restructuring during theOrdovician biodiversifications.

Data and Methods

Samples. Our data set includes 357 fossilcollections from the Ordovician of the UnitedStates (see Supplementary Table 1 online athttp://dx.doi.org/10.1666/07074.s1) that meetthe following criteria:

1. Collected from units representing shallowto deep subtidal (above storm wave base)mixed carbonate-clastic depositional envi-ronments.

2. High stratigraphic resolution (single bed orsmall group of beds).

3. Counts of all shelly macrofaunal elementsreported, all trilobites and rhynchonelli-form brachiopods identified at least to ge-nus, minimum sample size of 20 individu-als (median � 61, mean � 78, max � 554).

4. Good preservation quality (original shellcalcite in most brachiopod and trilobitetaxa).

The database contains extensive collectionsfrom the type areas of each of the four strati-graphic series of the Ordovician System inNorth America: our own Ibexian (Lower Or-dovician) and Whiterockian (Middle Ordovi-cian) collections from Utah and Nevada, andpublished data sets from the type Mohawkian(lower Upper Ordovician) in New York (Titus1986; Titus and Cameron 1976) and the typeCincinnatian (upper Upper Ordovician) inKentucky and Ohio (Holland and Patzkowsky2004). Additional published data sets are in-cluded from the Ibexian of central New York(Westrop et al. 1993) and the Mohawkian–Cin-cinnatian of western Virginia (Springer 1982)and Tennessee (Patzkowsky and Holland

344 SETH FINNEGAN AND MARY L. DROSER

1999). Although the Lower-Middle Ordovi-cian strata of the western United States andthe Upper Ordovician strata of the easternUnited States represent different tectonic set-tings, both were at tropical to subtropical lat-itudes throughout the Ordovician and bothrepresent mixed carbonate-clastic ramp andplatform depositional settings (Brett et al.2004; Ross et al. 1989). Moreover, data setsfrom these regions have been the basis formany previous studies of Ordovician paleo-ecological trends in North America, and havefigured particularly prominently in studiessuggesting that the ecological significance oftrilobites declined through the Ordovician(Sepkoski and Sheehan 1983; Sepkoski andMiller 1985; Miller et al. 1998; Peters 2004; Fin-negan and Droser 2005).

The following temporal bins were used,based primarily on the timescale of Ross andRoss (1995): Ibexian 1 (Skullrockian–Tulean,489.0–476.5 Ma), Ibexian 2 (Blackhillsian,476.5–472 Ma), Whiterockian 1 (zone L ofRoss et al. 1997, 472–470 Ma), Whiterockian 2(zones M–O of Ross et al. 1997, 470–460.5 Ma),Mohawkian 1 (Ashbyan–Rocklandian, 460.5–454.5 Ma), Mohawkian 2 (Kirkfieldian–Sher-manian, 454.5–451 Ma), Cincinnatian 1 (Ed-enian, 451–448.5 Ma), and Cincinnatian 2(Richmondian–Maysvillian, 448.5–444 Ma).

Abundance. For our Lower and Middle Or-dovician collections, we calculated abundanceas the minimum number of individuals ofeach genus present in each collection, follow-ing the protocols outlined by Gilinsky andBennington (1994). Minimum numbers of in-dividuals were also reported in most of theUpper Ordovician collections that we com-piled from the literature; in the few cases forwhich no information on counting methodwas given, we assumed that that the reportedcounts represented minimum numbers of in-dividuals. Determining minimum numbers ofindividuals is relatively straightforward forbrachiopods, as they produce only two skele-tal elements and all skeletal elements repre-sent a dead individual. However, it is moredifficult for trilobites. Trilobites produce mul-tiple skeletal elements, but only some of these(the cephalon and sometimes the pygidium)are typically counted by workers seeking to

estimate the minimum number of individuals.Thus, it is possible that trilobites are some-what underreported in many collections rel-ative to brachiopods. This may particularly bethe case for species of the exceptionally largeMiddle–Late Ordovician genus Isotelus (seebelow for further discussion), which is oftenrepresented by highly fragmented shell ele-ments. On the other hand, because trilobitesgrew by periodic molting, a given trilobite in-dividual could produce multiple shell ele-ments throughout its lifetime. Hence, the rel-ative abundance of trilobite skeletal materialin death assemblages may be inflated com-pared to the relative abundance of trilobite in-dividuals in the communities from which theyderive (following previous workers, we makethe simplifying assumption that on average alltrilobite individuals produced an equal num-ber of molts over their lifetime). These com-plications make it difficult to directly evaluatethe abundance of trilobite individuals in anycollection, but if they apply uniformly to allcollections in the data set then overall trendsin the abundance of skeletal elements shouldbe a reasonable proxy for trends in the num-ber of individuals.

Population density (abundance with respectto area or volume) is the most energeticallymeaningful measure of abundance, but suchdata are almost never available for fossil col-lections and are subject to severe taphonomiclimitations. We therefore use relative abun-dance as a proxy for population density. Incalculating relative abundance we included allcommonly reported shelly macrofauna (trilo-bites, articulate and inarticulate brachiopods,mollusks, echinoderms, bryozoans, and ru-gose corals, plus various minor groups). Weexcluded ostracods because of their small size,often extremely high abundance, and incon-sistent reporting in faunal lists. Relative abun-dances were normalized for all figures usingthe standard logit transform for proportionaldata.

Because it is measured with respect to thenumber of individuals sampled, any analysisof trends in relative abundance must implic-itly assume that total population density—thecombined number of individuals belonging toall groups of interest—is constant through the


FIGURE 1. Measurements taken on trilobite and bra-chiopod specimens, and illustrations of the biovolumeellipsoids constructed from those measurements. Forbrachiopods, the ellipsoid radii were calculated by halv-ing the length, width, and height measurements. Widthand height radii were calculated in the same manner fortrilobites, but because the length of the cephalon is onlya fraction of the length of an articulated individual, theradius of the length dimension was determined by mul-tiplying the length of the cephalon by a constant (seetext) and dividing by two.

sampled interval (Finnegan and Droser 2005).Given the great increase in diversity of benthicanimals during the Ordovician Period, this as-sumption is very likely invalid in this case.Even if the absolute abundance of trilobiteswere invariant through the Ordovician, an in-crease in the total density of all benthic ani-mals would have the effect of lowering the rel-ative abundance of trilobites through numer-ical dilution (Westrop and Adrain 1998a; Wes-trop et al. 1995). Therefore, the relativeabundance of trilobites in our Middle and es-pecially Late Ordovician samples should beregarded as a minimum estimate of trilobiteabundance. Although data normalization maylikewise distort the abundance trajectory ofbrachiopods somewhat, there is universalagreement that the average population densi-ty of brachiopods increased dramatically dur-ing the Ordovician (Harper et al. 2004b).

Body Size. Body volume estimates werebased on measurements of brachiopod pediclevalves and trilobite holaspid cranidia. ForLower and Middle Ordovician species, wemeasured specimens from our own samplesdirectly. Body sizes of Late Ordovician specieswere determined primarily from measure-ments of specimens in the collections of theMuseum of Comparative Zoology, HarvardUniversity. Whenever possible we measuredspecimens from the formations from whichsamples in our database derive, but in the fewcases in which such specimens were not avail-able we substituted conspecific or congenericspecimens from other units; excluding themhas little effect on observed trends. Two spe-cies (Bellefontia gyracantha and Clelandia parab-ola) from the Ibexian tribes Hill Formationwere measured from figured specimens pub-lished by Westrop et al. (1993). The number ofspecimens measured per species varied fromone to 34, depending on availability, with amedian of five for trilobites and nine for bra-chiopods. We made a special effort to measuremultiple specimens of larger species, becausethe range of body volumes is far greater thanin smaller species. The resulting averages arenecessarily approximations, but given thefive-order-of-magnitude variation in averagebody size in our data set it is highly unlikelythat this overwhelms the underlying trend.

It is common and often sufficient to use asingle length measurement as a proxy forbody size in analyses of evolutionary sizetrends, but it is important to have three-dimensional information for estimating indi-vidual biomass and energy use (EU), becauseof the cubic scaling of body volume with size.Multiplying anteroposterior length, trans-verse length, and dorsoventral length (here-after referred to as length, width, and height,respectively) captures most of the variation inbiovolume across larges size ranges (Novack-Gottshall 2008b); here we use a slightly dif-ferent approach, based on the same measure-ments, to model biovolume as an ellipsoidrather than a rectangular prism.

For brachiopods, length and width mea-surements on the pedicle valve, and the heightof the articulated shell, were used to generateellipsoids (Fig. 1) with a volume given by

(4/3)� (l/2)(h/2)(w/2), (1)

where l is the maximum length, w is the max-imum width, and h the maximum height ofthe articulated skeleton. In cases in which ar-ticulated specimens could not be measured,


we measured length and width on the pediclevalve and estimated height by using a height:width ratio generalized for different shellforms (concavo-convex, plano-convex, biocon-vex, or strongly biconvex). It should be notedthat this approach overestimates biovolume,because it assumes that the thickness of theshell itself is negligible and that the internalvolume of the shell is entirely filled with softtissues. In fact, brachiopod shells can be quitethick, especially in inflated forms, and muchof the internal volume of the shell is emptyspace. As long as the ratio of soft tissue toempty space is not size dependent, this doesnot introduce a systematic bias. An alternativeapproach, calculating biovolume simply asl ·w ·h, where h is not measured but is assumedto be constant across all sizes, results inchanges in the size ranking of some taxa (Sup-plementary Fig. 1A, online at http://dx.doi.org/10.1666/07074.s2) but gives very similarestimates of biomass and EU trends (Supple-mentary Fig. 1B,C).

For trilobites, cephalon length, width, andheight parameters were used to generate ellip-soids (Fig. 1). If the entire cranidium wasavailable, measurements were based on it. Thelength of the whole organism was estimatedas a multiple of the cranidium length, withdifferent multipliers used depending on over-all shape (i.e., long and thin versus short andbroad). Similarly, when the height of the ce-phalon could not be accurately measured,height was estimated based on the degree ofconvexity (for example, a height:width ratio of1:3 was used for the relatively inflated ‘‘Illaen-iform’’ species, whereas a ratio of 1:6 was usedfor relatively flattened ‘‘Oleniform’’ species,and intermediate ratios for species falling be-tween these end-members). Using a more gen-eralized approach that assumes the same rel-ative dimensions for all trilobites does notsubstantively change our results. As with thebrachiopods, our approach overestimates bio-volume, because the soft tissues of trilobiteswere generally concentrated in the axial lobeand the thin walking legs (Bambach 1993),with much of the remaining space enclosed bythe exoskeleton relatively empty. We make thesimplifying assumption that the ratio of softtissue biomass to empty space was broadly

similar in trilobites of all sizes. Although thereis certainly considerable uncertainty in thesize estimates derived from our geometricalapproximations, even a factor of two or threeerror is minor compared to the multiple order-of-magnitude variation in body size exhibitedby both trilobites and brachiopods in our dataset.

Average body size was calculated as thearithmetic average volume of all individualsfor each species. Average body size ratherthan median body size is the appropriate met-ric for this study, because large individuals ac-count for biomass and energy use out of pro-portion to their abundance. In the rare casesin which no specimens of a species could bemeasured, that species was assigned the meanbody size for other species in the same classand time bin. All of these species are numer-ically rare, and excluding them rather than as-signing the average value has very little effecton observed trends.

Biomass. We estimate biomass from rela-tive abundance and body size. The biomass ofa taxon within a sample is determined simplyby multiplying its average body volume (weassume a linear relationship between bodyvolume and body mass) by its relative abun-dance:

Biomass � nm (2)

where m is the average body size of individualsin the population and n is the relative abun-dance of the species in the collection. We sumbiomass estimates for all taxa in the sample toproduce an estimate of the total relative bio-mass of each group represented in the sample.

Energy Use. Whereas biomass is a relative-ly straightforward function of abundance andbody mass, the energy required to sustain apopulation at equilibrium is a function ofabundance and individual metabolic rate.Metabolic rates are affected by physiologicaland behavioral attributes that cannot be mea-sured in fossil organisms, and are also influ-enced by ambient temperature (Gillooly et al.2001). For members of the same clade inhab-iting the same environment, however, thesevariables can largely be factored out. Withingroups as ecologically and physiologicallydisparate as plants, mammals, fish, aquatic in-


vertebrates, and protists, individual restingmetabolic rate has been shown to scale as ap-proximately the ¾ power of body mass (Gil-looly 2001; Banavar et al. 2002). A recently de-veloped general model uses this scaling rela-tionship and biochemical kinetics to predictmetabolic rate as a function of body size andambient temperature (Gillooly 2001). Thismodel has the form:

�E/kT 3/4B(M, T) � B e M0 (3)

where B is individual resting metabolic rate, Eis the average activation energy of rate-limit-ing biochemical metabolic reactions, k is Boltz-mann’s constant, T is absolute temperature, Mis individual body mass, and B0 is a taxon-dependent normalization constant. Because itvaries only at high taxonomic levels, this con-stant can be factored out for estimating with-in-clade trends. Thus, a relative estimate of thepopulation energy use (EU), the aggregate met-abolic rate of individuals in the population(Savage 2004), is given by:

�1/kT 3/4EU(m, T) � e nm (4)

Because all samples come from tropical tosubtropical latitudes and relatively shallowwater, we initially assume constant tempera-ture (temperature sensitivity is considered be-low) so that equation (3) reduces to

3/4EU(m) � nm . (5)

We use this equation to derive relative EU es-timates for all trilobite and brachiopod speciesin each sample. As with biomass, EU estimatesare summed to produce an estimate of the to-tal EU of each group in each collection. Al-though we assume ¾ scaling of individualmetabolic rate with body size, assuming thealternative hypothesis of ⅔ scaling (Dodds etal. 2001) does not change the observed pat-terns significantly.

Predicted Abundance. The positive scalingof individual EU with body size imposes afundamental constraint on population densi-ty: if total energy availability is constantacross all body size classes, then populationdensity is expected to scale approximately asthe inverse of body size (Damuth 1981, 1987b;Brown 1995; Kerr and Dickie 2001; Cohen2003). Although the noise in this relationship

is very high, it provides a first-order predic-tion of the expected population density (N) ofa taxon:

�1/kT �3/4N(T) � B e m ,0 (6)

which reduces to

�3/4N � B m0 (7)

within a given environment with constanttemperature, and

�3/4N � m (8)

for taxa belonging to the same clade and in-habiting the same environment. It is not pos-sible to estimate relative abundances withoutsize data for all taxa in each collection (whichwe do not have), because the relative abun-dance of any taxon is influenced by the abun-dance of all other taxa in the collection. How-ever, the expected ratio of trilobite individualsto brachiopod individuals is dimensionlessand unaffected by the abundances of othertaxa. We therefore used equation (7) to predictthe trilobite:brachiopod ratio for each collec-tion only on the basis of the sizes of constit-uent taxa. Having no basis for estimating thenormalization constant (B0) for trilobites orbrachiopods, we make the simplifying as-sumption that it is the same for both of thesegroups. Difference in B0 would skew the ratioone way or another, but because all collectionswould be equally affected, this cannot distortpredicted trends in the ratio, which are our pri-mary concern.

Treatment of Missing Values. All of thestratigraphic units included in our analysisare known to contain both trilobites and bra-chiopods, but trilobites occur in only 63% ofLate Ordovician collections (versus 100% inthe Early Ordovician), and brachiopods occurin only 74% of Early Ordovician collections(versus �99% in the Late Ordovician). This isnot surprising: given the small size of manycollections, rare taxa are likely to go unsam-pled. To avoid the problems associated withzeroes in the data set (dividing by zero, orplotting zeroes on a logarithmic scale), zeroeswere assigned arbitrary values approximatelyone order of magnitude lower than the lowestactual value in the data set. Thus, if no bra-chiopods occurred in a collection it was as-


FIGURE 2. Temporal trends in the relative abundance oftrilobites (A) and brachiopods (B) in shallow to deepsubtidal mixed carbonate-clastic settings. The relativeabundance of each group is calculated as a proportionof all individuals in the collection (including trilobites,brachiopods, and other taxa). When either group wasentirely missing from a collection, it was arbitrarily as-signed a relative abundance of 0.001. Relative abun-dances for each group are logit-transformed. The endsof the boxes mark the positions of the first and thirdquartiles, horizontal lines mark the median, whiskersextend 1.5 times the interquartile range (IQR) below thefirst and above the third quartile. Open circles are col-lections that fall less than 1.5 · IQR above or below themedian; filled circles are outliers. Time bins are as fol-lows: Ibexian 1 � 489.0–476.5 Ma, Ibexian 2 � 476.5–472Ma, Whiterockian 1 � 472–470 Ma, Whiterockian 2 �470–460.5 Ma, Mohawkian 1 � 460.5–454.5 Ma, Mohaw-kian 2 � 454.5–451 Ma, Cincinnatian 1 � 451–448.5 Ma,Cincinnatian 2 � 448.5–444 Ma.

signed a brachiopod relative richness of 0.01,a relative abundance of 0.001, a biomass of0.01, an EU of 0.01, and a predicted popula-tion density of 0.0001. An alternative ap-proach is to combine collections by formationand calculate relative abundance, biomass,and EU from these pooled collections. Thissubstantially reduces the number of datapoints but eliminates the need to account formissing values. Trends observed in pooledcollections are very similar to those observedwhen all collections are treated independent-ly.

Results

Consistent with previous studies, the aver-age relative abundance of trilobites decreasesby an order of magnitude between the EarlyOrdovician (I1–I2) and the Late Ordovician(M1–C2), whereas that of brachiopods in-creases (Fig. 2A,B). Trilobites constitute an av-erage 58% of individuals in Early Ordoviciancollections, but only 4% of individuals in theLate Ordovician, whereas brachiopods gofrom an average of 19% in the Early Ordovi-cian to 77% in the Late Ordovician. Relativegenus richness trends are similar (Fig. 3A,B),though because of the low richness of all taxain most samples (median genus richness � 6),they vary over a comparatively limited range.

The average body sizes of both trilobitesand brachiopods increase substantially throughthe Ordovician (Churchill-Dickson 2001;Stempien et al. 2005; Novack-Gottshall 2008a)and this is expressed in our data set (Fig.4A,B). Consequently, trends in biomass departquite strikingly from relative richness andabundance trends (Fig. 5A,B). Most notably,the sharp decline in relative abundance of tri-lobites is not mirrored by biomass estimates:though total within-sample trilobite biomassvaries over five orders of magnitude in thesample set as a whole, the average biomass oftrilobites in Late Ordovician collections iswithin an order of magnitude of the Early Or-dovician average.

The sharp increase in average trilobite bodysize in the upper Middle and Late Ordovicianis largely attributable to the widespread oc-currence of the exceptionally large asaphidgenus Isotelus. This exclusively Laurentian ge-

nus includes the largest known trilobite spe-cies (I. rex), which attained lengths of up to 72cm (Rudkin et al. 2003). Though this speciesdoes not appear in our data set, the four spe-


FIGURE 3. Temporal trends in the relative genus rich-ness of trilobites (A) and brachiopods (B) in shallow todeep subtidal mixed carbonate-clastic settings. The rel-ative richness of each group is calculated as a proportionof all genera in the collection (including trilobites, bra-chiopods, and other taxa). When either group was en-tirely missing from a collection, it was arbitrarily as-signed a relative richness of 0.01. Relative richnesses foreach group are logit-transformed Boxes, whiskers, cir-cles, and time bins as in Figure 2.

FIGURE 4. Temporal trends in the body size distribu-tions and relative abundances of trilobites (A) and bra-chiopods (B) in shallow to deep subtidal mixed carbon-ate-clastic settings. The vertical axis is log10 estimatedbiovolume, and the bubble marking the position of eachspecies is scaled to its average relative abundance in col-lections. The prominent gap in trilobite body size dis-tribution during the Late Ordovician occurs betweenvery large Isotelus species and moderate-sized ceraurid,calymenid, and proetid species. Time bins as in Figure 2.

cies that do, I. gigas, I. copenhagenensis, I. bra-chycephalus, and I. maximus—though I. brachy-cephalus and I. maximus are rarely differenti-ated in published data sets and may not in factbe discrete species (Rudkin et al. 2003)—all at-tain average body sizes nearly two orders ofmagnitude above the median trilobite bodysize. Unsurprisingly given the expected in-verse relationship between body mass andpopulation density, these trilobites are com-paratively uncommon (Fig. 4A) and are ab-

sent in many samples from stratigraphic unitsin which they are known to occur. Neverthe-less, they constitute a large proportion of alltrilobite individuals in late Middle and LateOrdovician samples and their average size issuch that the average biomass of Late Ordovi-cian samples is comparable to that of EarlyOrdovician samples even when these absencesare included.

The average estimated EU of trilobites alsoshows no secular trend (Fig. 6A), whereas that


FIGURE 5. Temporal trends in the estimated standingbiomass of trilobites (A) and brachiopods (B) in shallowto deep subtidal mixed carbonate-clastic settings. Bio-mass is calculated as mean body size multiplied by rel-ative abundance, and the resulting biomass estimatesare summed for all taxa in each group. If a group wasentirely missing from a collection, it was arbitrarily as-signed a biomass of 0.01. Boxes, whiskers, circles, andtime bins as in Figure 2.

FIGURE 6. Temporal trends in the estimated energy use(EU) of trilobites (A) and brachiopods (B) in shallow todeep subtidal mixed carbonate-clastic settings. EU iscalculated as mean body size to the ¾ power multipliedby relative abundance, and the resulting EU estimatesare summed for all taxa in each group. If a group wasentirely missing from a collection, it was arbitrarily as-signed an EU of 0.01. Boxes, whiskers, circles, and timebins as in Figure 2.

of brachiopods increases substantially (Fig.6B). In estimating EU, however, the tempera-ture-sensitivity of metabolic efficiency (eq. 3)introduces a complicating factor. We haveminimized the effects of latitudinal variation inour data set by including only collections fromtemperature-sensitive, carbonate-dominateddepositional settings within tropical to sub-tropical latitudes, but there is considerable ev-idence of a long-term cooling trend through-out much of the Late Ordovician of Laurentia(Patzkowsky et al. 1997; Pope and Steffen

2003; Herrmann et al. 2004; Saltzman andYoung 2005), and several of the Late Ordovi-cian units sampled in our database have beeninterpreted as cool-water carbonates (Popeand Read 1995; Holland and Patzkowsky1996). The earliest evidence of significant cool-ing in Laurentia occurs in the late Mohawkian(Pope and Steffen 2003; Saltzman and Young2005) and includes a shift to more positive�18O and �13C values (Shields et al. 2003), ex-pansion of cherts and other upwelling-asso-ciated lithologies along the southern margin,


FIGURE 7. Impact of a hypothetical 10�C cooling in themid-Mohawkian on estimated energy use of trilobites(A) and brachiopods (B). Open boxes represent the ob-served trend if a uniform average temperature of 27�Cis assumed; filled boxes represent the trend if an averagetemperature of 17�C is assumed from the mid-Mohaw-kian on. The vertical axis is scaled by multiplying EU bye�1/kT, and hence the units are arbitrary. Boxes, whiskers,and time bins as in Figure 2.

and a shift from tropical to temperate-typecarbonate sedimentation in the Taconic fore-land and adjacent cratonic seaway. Ocean cir-culation models suggest that average sea-sur-face temperatures along the southern marginof Laurentia and in the interior seaway mayhave been as low as 18–20�C (Herrmann et al.2004), despite its tropical-to-subtropical po-sition. Assuming, by comparison with mod-ern tropical seas, an average sea-surface tem-perature of 27�C during deposition of Ibexian-Whiterockian and lower Mohawkian tropicalcarbonates, this suggests a 7–9�C cooling inthe Late Mohawkian. We use equation (4) toevaluate the effect of a 10�C cooling on series-level trends in trilobite EU (Fig. 7).

This has some effect on estimated EU trendsfor both trilobites and brachiopods. Under thismodel, trilobites show a slight decline in es-timated EU (Fig. 7A), though the decline isneither as coherent nor as large in magnitudeas the decline in relative abundance (Fig. 2A).The estimated EU of brachiopods remainsfairly constant from the Whiterockian on un-der this model (Fig. 7B), whereas under theconstant temperature model there is a distinct,sustained increase from the Middle (W1–W2)to the Late (M1–C2) Ordovician. These resultsare suggestive, but we emphasize that thismodel builds in multiple assumptions andsimplifications regarding quite poorly con-trolled variables, and hence should be viewedwith a good deal of skepticism. We also pointout that trilobite biomass estimates remainroughly constant, and brachiopod biomass es-timates increase significantly, from the lateMiddle Ordovician (W2) to the early Late Or-dovician (M1). Coming as this does before theonset of mid-Mohawkian cooling, it suggeststhat cooling by itself does not provide an ad-equate explanation for the observed trends.

The increasing average body size of trilobiteindividuals raises the possibility that the de-clining relative abundance of trilobites in thisdata set is, in part, a consequence of the in-verse association between abundance andbody size. This can be evaluated by comparingthe observed trend in the ratio of trilobite tobrachiopod individuals to the trend predictedby body size (eq. 7). As a comparison, we alsocalculated the ratio of trilobite to brachiopod

genera in each collection; this gives the ex-pected ratio of trilobite to brachiopod individ-uals if all taxa are represented by equal num-bers of individuals (i.e., evenness � 1), withno association between size and abundance.

The trends in average trilobite:brachiopodratio predicted by the size-dependent andsize-independent approaches are both closelycorrelated with the observed trend (Fig. 8);however, the slope is much closer to one whenthe average trilobite:brachiopod ratio is re-gressed on the average ratio predicted by the


FIGURE 8. The average ratio of trilobite individuals tobrachiopod individuals for each time bin plotted againstthe average ratio of trilobite genera to brachiopod gen-era (A) and against the average ratio of trilobite indi-viduals to brachiopod individuals predicted by bodysize distributions (B). Bars represent 95% confidence in-tervals for the mean. Body size and richness provide abetter prediction of abundance trends than does rich-ness alone.

size-dependent model than it is when the av-erage trilobite:brachiopod ratio is regressedon the average ratio predicted by the size-independent model. The size-independentmodel significantly underestimates the mag-nitude of the decrease in the trilobite:brachio-pod ratio between the Early and Late Ordo-vician, whereas the size-dependent modelpredicts it accurately. The size-dependentmodel does have an intercept significantlygreater than zero, indicating that it consis-

tently overestimates the trilobite:brachiopodratio, especially in the Early Ordovician. Thissuggests that the normalization factor associ-ated with size-abundance scaling may behigher for brachiopods than for trilobites.

Discussion

Preservation of Abundance–Body Size Relation-ships. Abundance and body size patterns inmodern clades and ecosystems are a conten-tious subject in part because accurate mea-surement is difficult (Blackburn and Gaston1997), and such problems are obviously com-pounded in the fossil record. Time-averaging,transport, and differential preservation poten-tial, life span, and mode and rate of shell pro-duction all have potentially severe effects onthe ecological fidelity of abundance and bodysize data in fossil assemblages. Nonetheless,live-dead comparisons of mollusk communi-ties have shown surprisingly strong agree-ment in rank-order abundance between skel-etal assemblages and the communities fromwhich they derive (Kidwell 2001, 2002), sug-gesting that at least within single clades it maybe possible to track abundance trends in thefossil record. Brachiopods are good candi-dates for such study because of their relativelydurable low-organic calcite shells. Trilobitesare also readily preservable, but interpretationof trilobite abundance trends is complicatedby the fact that they regularly molted as theygrew. It is unclear how this should affect size-abundance relationships—on one hand,smaller species are likely to have had shortergeneration times and thus to have contributeddisproportionately to time-averaged shell ac-cumulations; on the other hand, larger specieswere likely longer-lived and thus presumablyproduced more molts per individual overtheir lifetime. This issue may ultimately be ad-dressed by comparing abundance to estimat-ed growth rate in species for which both typesof data are available, but in the absence of suchdata we assume that total molt contribution isinvariant with respect to body size.

One of the most fundamental aspects of eco-system structure is that maximum populationdensity decreases as a function of body size—on average, small organisms are more numer-ous than large ones. This relationship, appar-


FIGURE 9. Logit-transformed relative abundance ver-sus log-transformed average body size for all trilobiteand brachiopod occurrences in the data set. There is aweak but significant negative association between bodysize and relative abundance (slope � �0.46, p � 0.009).

FIGURE 10. Histogram of Spearman rs values for thecorrelation between body size and rank abundance forall collections containing at least four trilobite and/orbrachiopod genera. Negative rs scores are significantlymore common than positive scores, indicating that theexpected scaling of abundance with body size is pre-served in the majority of collections. Black bars repre-sent rs score that are significant at the 95% confidencelevel, and gray bars represent insignificant scores. Thelow proportion of significant scores is expected giventhe small numbers of taxa in most collections.

ent in a wide array of marine and terrestrialecosystems, reflects fundamental energeticconstraints imposed by the positive scaling ofindividual EU with body size (Damuth 1981,1987b; Brown 1995; Kerr and Dickie 2001; Co-hen 2003). Thus, examining the relationshipbetween body size and relative abundance inour data set constitutes a simple test of itsfirst-order ecological fidelity. Plotting the logitof relative abundance against the log of meanbody size for all occurrences in the data set(Fig. 9) suggests that there is a signal, howeverdegraded, of original abundance structure.Although variance is very high and most taxatend to be rare in all size classes, both maxi-mum and average relative abundance de-crease with increasing body size. A permuta-tion test on the slope of this relationship(��0.46) shows that it is significantly nonran-dom (p � 0.009), although the difference inunits (logit abundance versus log biovolume)makes it difficult to directly compare thisslope to the �¾ log-log slope predicted by theenergetic equivalence rule.

The small size of most collections in our da-tabase (median number of individuals � 61)constrains relative abundance to vary onlyover two orders of magnitude whereas bodysizes span six orders of magnitude, making it

difficult to test for specific scaling relation-ships. Variation in sample size also introducessignificant noise into relative abundance pat-terns: the relative abundance of the rarest tax-on in a collection of 50 individuals may be anorder of magnitude higher than the relativeabundance of the rarest taxon in a collectionof 500 individuals. An alternative approachthat eliminates this problem is to test for size-structuring within each collection, rather thanamong all taxon occurrences collectively. Wetherefore calculated Spearman rank-ordercorrelation coefficients (rs) for the associationbetween relative abundance and mean bodysize for each collection that included at leastfour brachiopod and/or trilobite taxa. If thereis no inverse association between abundanceand size, rs values should show a mode cen-tered on zero. There is, however, a clear ten-dency toward negative rs scores: 64% of allcollections have negative rs scores, and thisfigure rises to 83% if only statistically signifi-cant rs scores are considered (Fig. 10). The po-tential for size-related biasing of relativeabundance patterns in the fossil record is an


FIGURE 11. Temporal trends in the estimated standingbiomass of trilobites (A) and brachiopods (B) in shallowsubtidal collections only. Biomass calculated as in Figure4; boxes, whiskers, circles, and time bins as in Figure 2.

FIGURE 12. Temporal trends in the estimated standingbiomass of trilobites (A) and brachiopods (B) in deepsubtidal collections only. Biomass calculated as in Fig-ure 4; boxes, whiskers, circles, and time bins as in Figure2.

important subject for more detailed investi-gation with larger collections, but at presentwe see little evidence that abundance trends inthis data set are significantly size-biased.

Environmental Coverage. Our data set is in-tentionally limited to mixed carbonate-clasticunits above maximum storm wave base, and itexcludes the deep slope and basinal environ-ments in which trilobites may have remaineddominant elements of the fauna into the LateOrdovician (Sepkoski and Sheehan 1983; Sep-koski and Miller 1985). Within this relativelynarrow range bathymetric coverage is un-even—most Early Ordovician collections rep-resent shallow subtidal environments (abovenormal wave base), whereas most Late Ordo-

vician collections are from deep subtidal col-lections (between normal wave base and max-imum storm wave base). Both shallow anddeep subtidal collections show similar trendsin estimated biomass, however (Figs. 11, 12),and hence it is unlikely that the compositetrend is strongly influenced by environmentalheterogeneity.

Geographic Coverage and Generality of Re-sults. Many of the units that have figured inprevious studies of Ordovician paleoecologi-cal trends and evolutionary faunas are includ-ed in our database. Coverage of the Upper Or-dovician strata of the Appalachian forelandand adjacent cratonic sea is particularly


heavy. The richly fossiliferous rocks of this re-gion contain a quite low-diversity and low-abundance trilobite fauna (only nine generaoccur in our Mohawkian data set, and sevenin the Cincinnatian), and this paucity has beenthe basis for previous suggestions that the eco-logical significance of trilobites decreasedthrough the Ordovician (Miller et al. 1998).Thus, although it is geographically limited totwo broad regions, the data set is appropriatefor testing this hypothesis. Suitable whole-fauna abundance and body size data are notavailable from other well-studied Upper Or-dovician strata in Canada and the MidwesternUnited States (Westrop and Adrain 1998a; Ad-rain et al. 2000; Hunda et al. 2003; Amati2004), but given the comparatively high spe-cies richness of trilobites in these units it is un-likely that the relative abundance of trilobitesis lower than it is in the eastern United States.

It is also noteworthy that moderately to ex-tremely large species of Isotelus occur in manyof these units, including the largest trilobiteever described, I. rex, in the Cincinnatian ofManitoba (Rudkin et al. 2003). The temporaland geographic distribution of large Isotelusspecies in eastern North America has been re-cently reviewed (Rudkin et al. 2003); in theCordilleran belt, several Middle and Late Or-dovician Isotelus species are known from silic-ified material (Chatterton and Ludvigsen1976; Ross et al. 1980; Hunda et al. 2003) thatoften consists primarily of small early onto-genetic stages, so that the average adult sizeof these species cannot be reliably estimatedfrom published plates. Exceptionally largespecies are present in at least some Cordille-ran units—for instance the Whiterockian toearly Mohawkian species I. copenhagenensis,which occurs in our collections from Nevada,attained a maximum length of at least 20 cm,according to extrapolation from a figured py-gidium (Ross and Shaw 1972).

Implications for Ordovician Trends in AnimalBiomass. Bambach (1993) argued that the ag-gregate standing biomass of marine inverte-brates has increased through the Phanerozoic.Although he did not specifically discuss bio-mass increase in the Ordovician, our results,along with other recent work (Novack-Gottsh-all 2008a) suggest that the dramatic increase

in the diversity of skeletonized marine inver-tebrates during the Ordovician was accom-panied by a substantial increase in theirstanding biomass. Our data are obviously lim-ited to two well-skeletonized groups, but theOrdovician increase in the depth and intensityof bioturbation (Droser and Bottjer 1989) is ev-idence that the biomass of soft-bodied infau-nal burrowers also increased. Whether thistrend reflects an increase in overall primaryproductivity, in the nature of primary pro-ducers, or in the metabolic efficiency of con-sumers (Payne and Finnegan 2006) remains anopen question.

Implications for the Nature of Ordovician Eco-logical Restructuring. Our results provide lit-tle support for the hypothesis that trilobiteswere in any way actively displaced from ben-thic habitats by the expansion of the PaleozoicFauna. Because of an increase in the averagebody mass of sampled individuals, estimatesof the most fundamental metrics of ecologicalsignificance—biomass and energy use—arefairly constant for trilobites despite an order-of magnitude decline in the relative abun-dance of this group. This does not necessarilyimply that there were no significant ecologicalinteractions between trilobites and membersof the Paleozoic EF (or for that matter, theModern EF). Any such interactions would al-most necessarily have been rather diffuse,however—there is little evidence of predator-prey interactions, and trilobites occupied aquite different region of ecospace than themembers of the Paleozoic EF, most of whichwere sessile suspension feeders (Bush et al.2007; Novack-Gottshall 2007). Given this, wefavor the interpretation that the Paleozoic EFdiversified not by outcompeting the CambrianEF but by evolving to take advantage of re-sources (particulate organic matter in the wa-ter column, in particular) that were underuti-lized by the members of the Cambrian EF.

The trend in body size distribution of tri-lobites in our data set does suggest the pos-sibility that the ecological roles of trilobitesmay have changed quite significantly duringthe Ordovician, a notion that is also supportedby other lines of evidence. Foote (Foote 1991;Miller and Foote 1996) found that the mor-phological diversity of trilobites increased sig-


nificantly between the Early and Late Ordo-vician, suggesting a comparable increase inecological diversity. Fortey and Owens (1999)have made the functional morphological ar-gument that trilobites with hypostomes lack-ing a skeletal attachment to the cranidiumwere likely detritivores, whereas those withhypostomes firmly braced against the crani-dium were probably predators and scaven-gers. The former group taxonomically and nu-merically dominates many trilobite commu-nities in the Middle–Late Cambrian and EarlyOrdovician, but trilobites with attached hy-postomes (of which Isotelus is a particularlywell-known example) are taxonomically dom-inant by the Late Ordovician. If Fortey andOwens’ model is correct, this trend implies anincrease in mean trophic level for the clade asa whole during the Ordovician. Because lessenergy is available at higher trophic levels thiswould, all else being equal, force a decline inabundance even in the absence of a trend to-ward larger body sizes. However, absent bet-ter information about both trilobite feedinghabits and Ordovician productivity trends,this line of argument remains speculative.

Our data set is restricted to two broad geo-graphic regions and a narrow range of envi-ronments, and hence it is not sufficient to gen-eralize about clade-level body size trends. Butrecent studies of continental and global-scalebody size distributions have found significantincreases in the average body size of trilobites(Churchill-Dickson 2001, personal communi-cation 2005; Novack-Gottshall 2008a), brachio-pods (Harper et al. 2004a; Stempien et al.2005), and bivalves (Stempien et al. 2005)through the Ordovician. Brachiopods also di-versify explosively (Harper et al. 2004a) andbivalves diversity steadily (Miller and Sepko-ski 1988) through this interval, but both the al-pha (within-habitat) and global genus diver-sity of trilobites remains roughly invariant(Westrop and Adrain 1998a; Adrain et al.2000; Sepkoski 2002). Despite two major fam-ily-level turnover pulses within the Ordovi-cian (Adrain et al. 2004), trilobite communitiesappear to have been ‘‘species-saturated’’—ator near carrying capacity—from the MiddleCambrian through the mid-Silurian, except-

ing depauperate post-extinction communities(Adrain et al. 2000).

Together with the increase in average bodysize, this saturation suggests a novel expla-nation for the apparent decline in trilobiteabundance. An increase in average cranidiumlength from 6.5 mm to 9.5 mm, observedin multiple Laurentian families (L. Churchill-Dickson personal communication 2005) can beextrapolated with the geometrical approxi-mations discussed above to a roughly three-fold increase in average body mass. Assuming¾ power scaling of individual metabolic ratewith body size and constant food availability,a threefold increase in body mass would nec-essarily be accompanied by a 57% decreasein population density ([1/3]3/4 � .43). Thus, itmay be that the declining abundance of trilo-bites in the Ordovician is at least in part a sim-ple consequence of Cope’s Rule—the frequent-ly observed tendency of lineages to increase insize through time (Stanley 1973; Jablonski1996). This suggestion is quite speculative, butthe general relationships among body size, di-versity, and abundance trends over macroevo-lutionary time scales are intriguing areas forfurther research.

Summary

The well-documented Ordovician decline inthe relative abundance of trilobites in shallowto deep subtidal level-bottom assemblages(Fig. 2) is not paralleled by estimates of trilo-bite biomass or energy use (Figs. 5, 6), whichinstead show relative stability throughout theOrdovician. This stability is attributable to theincreasing average body size of trilobites (Fig.4), and in particular the widespread occur-rence of species of the genus Isotelus in Middleand Late Ordovician collections. Brachiopodsshow increases in relative abundance, rich-ness, mean body size, and estimated biomassand energy use throughout the Ordovician.There is thus little evidence that, at the locallevel, the expansion of the brachiopods andother members of the Paleozoic EvolutionaryFauna came at the expense of trilobites in Lau-rentia. Rather, the aggregate standing biomassof benthic communities increased as the bio-mass (and by inference the energy use) of tri-lobites remained approximately constant and


that of Paleozoic EF members rose substan-tially. Although they show no strong trend instanding biomass or inferred energy use, oth-er lines of evidence do suggest that trilobiteswere active participants in Ordovician biodiv-ersification, evolving new morphologies andnew ecological strategies over the course ofthe interval. These data demonstrate that tem-poral trends in biomass may be substantiallydecoupled from trends in relative abundance,and hence caution should be used in drawingexplicit or implicit energetic inferences fromabundance data alone.

Acknowledgments

We wish to thank R. Bambach, R. Gaines, N.Hughes, and J. Payne for very helpful discus-sions. We also thank all of the workers whoproduced data sets included in our analysis,particularly S. Holland, M. Patzkowsky, D.Springer, R. Titus, and S. Westrop. This man-uscript benefited from very thoughtful re-views by M. Patzkowsky and P. Sheehan. Weare grateful to F. Collier and J. Cundiff fortheir assistance with examining samples andspecimens in the collections of the Museum ofComparative Zoology at Harvard. This workwas partially supported by National ScienceFoundation grant EAR-9219731 to M.L.D. Thisis Paleobiology Database contribution number77.

Literature CitedAdrain, J. M., S. R. Westrop, B. D. E. Chatterton, and L. Ram-

skold. 2000. Silurian trilobite alpha diversity and the end-Or-dovician mass extinction. Paleobiology 26:625–646.

Adrain, J. M., G. D. Edgecombe, R. A. Fortey, O. Hammer, J. R.Laurie, T. McCormick, A. W. Owen, B. G. Waisfeld, B. D. Web-by, S. R. Westrop, and Z.-y. Zhou. 2004. Trilobites in Webby etal. 2004.

Amati, L. 2004. Systematics and paleoecology of trilobites fromthe Late Ordovician Viola Group, south-central Oklahoma.Ph.D. dissertation. University of Oklahoma, Oklahoma City.

Bambach, R. K. 1983. Ecospace utilization and guilds in marinecommunities through the Phanerozoic. Pp. 719–746 in M. J. S.Tevesz and P. L. McCall, eds. Biotic interactions in recent andfossil benthic communities. Plenum, New York.

———. 1985. Classes and adaptive variety: the ecology of di-versification in marine faunas through the Phanerozoic. In J.W. Valentine, ed. Phanerozoic diversity patters: profiles inmacroevolution. Princeton University Press, Princeton, N.J.

———. Seafood through time: changes in biomass, energetics,and productivity in the marine ecosystem. Paleobiology 19:372–397.

Banavar, J. R., J. Damuth, A. Maritan, and A. Rinaldo. 2002. Sup-ply-demand balance and metabolic scaling. Proceedings ofthe National Academy of Sciences USA 99:10506–10509.

Benton, M. J. 1996. On the nonprevalence of competitive re-placement in the evolution of tetrapods. Pp. 185–210 in Ja-blonski et al. 1996.

———. 1997. Models for the diversification of life. Trends inEcology and Evolution 12:490–495.

Blackburn, T. M., and K. J. Gaston. 1997. A critical assessmentof the form of the interspecific relationship between abun-dance and body size in animals. Journal of Animal Ecology66:233–249.

Brett, C. E., P. I. McLaughlin, S. R. Cornell, and G. C. Baird. 2004.Comparative sequence stratigraphy of two classic Upper Or-dovician successions, Trenton Shelf (New York-Ontario) andLexington Platform (Kentucky-Ohio): implications for eustasyand local tectonism in eastern Laurentia. Palaeogeography,Palaeoclimatology, Palaeoecology 210:295–329.

Brown, J. H. 1995. Macroecology. University of Chicago Press,Chicago.

Bush, A. M., R. K. Bambach, and G. M. Daley. 2007. Changes intheoretical ecospace utilization in marine fossil assemblagesbetween the mid-Paleozoic and late Cenozoic. Paleobiology33:76–97.

Chatterton, B. D. E., and R. Ludvigsen. 1976. Silicified MiddleOrdovician trilobites from the South Nahanni River area, Dis-trict of Mackenzie, Canada. Palaeontographica, Abteilung A154:1–106.

Churchill-Dickson, L. 2001. Late Ordovician increase in trilobitesize and its evolutionary implications. PaleoBios 21:41–42.

Cohen, J. E. 2003. Ecological community description using thefood web, species abundance, and body size. Proceedings ofthe National Academy of Sciences USA 100:1781.

Damuth, J. 1981. Population-density and body size in mammals.Nature 290:699–700.

———. 1987a. Interspecific allometry of population-density inmammals and other animals: the independence of body-massand population energy-use. Biological Journal of the LinneanSociety 31:193–246.

———. 1987b. Interspecific allometry of population density inmammals and other animals. Biological Journal of the Lin-nean Society 31:193–246.

Dietl, G. P., and G. J. Vermeij. 2006. Comment on ‘‘Statistical In-dependence of Escalatory Ecological Trends in PhanerozoicMarine Invertebrates.’’ Science 314:925e-.

Dodds, P. S., D. H. Rothman, and J. S. Weitz. 2001. Re-exami-nation of the ‘‘3/4-law’’ of metabolism. Journal of TheoreticalBiology 209:9–27.

Droser, M. L., and D. J. Bottjer. 1989. Ordovician increase in ex-tent and depth of bioturbation—implications for understand-ing early Paleozoic ecospace utilization. Geology 17:850–852.

Finnegan, S., and M. L. Droser. 2005. Relative and absoluteabundance of trilobites and rhynchonelliform brachiopodsacross the Lower/Middle Ordovician boundary, eastern Basinand Range. Paleobiology 31:480–502.

Foote, M. 1991. Morphological patterns of diversification: ex-amples from trilobites. Palaeontology 34:461–485.

Fortey, R. A., and R. M. Owens. 1999. Feeding habits in trilo-bites. Palaeontology 42:429–465.

Gilinsky, N. L., and J. B. Bennington. 1994. Estimating numbersof whole individuals from collections of body parts: a taph-onomic limitation of the paleontological record. Paleobiology20:245–258.

Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and E. L.Charnov. 2001. Effects of size and temperature on metabolicrate. Science 293:2248–2251.

Gould, S. J., and C. B. Calloway. 1980. Clams and brachiopods:ships that pass in the night. Paleobiology 6:383–396.

Harper, D. A. T., L. R. M. Cocks, L. Popov, P. M. Sheehan, M. G.Basset, P. Copper, L. E. Holmer, J. Jin, and J. Rong. 2004a. Bra-chiopods. Pp. 157–178 in Webby et al. 2004.


Harper, D. A. T., L. R. M. Cocks, L. M. Popov, P. M. Sheehan, M.G. Basset, P. Copper, L. Holmer, J. Jisuo, and J. Rong. 2004b.Brachiopods. Pp. 157–178 in Webby et al. 2004.

Herrmann, A. D., B. J. Haupt, M. E. Patzkowsky, D. Seidov, andR. L. Slingerland. 2004. Response of Late Ordovician paleo-ceanography to changes in sea level, continental drift, and at-mospheric pCO2: potential causes for long-term cooling andglaciation. Palaeogeography, Palaeoclimatology, Palaeoecol-ogy 210:385–401.

Holland, S. M., and M. E. Patzkowsky. 1996. Sequence stratig-raphy and long-term paleoceanographic change in the Mid-dle and Upper Ordovician of the Eastern United States. Geo-logical Society of America Special Paper 306:117–129.

———. 2004. Ecosystem structure and stability; middle UpperOrdovician of central Kentucky, USA. Palaios 19:316–331.

Hunda, B. R., B. D. E. Chatterton, and R. Ludvigsen. 2003. Silic-ified Late Ordovician trilobites from the Mackenzie Moun-tains, Northwest Territories, Canada. Palaeontographica Can-adiana 21:87.

Jablonski, D. 1996. Body size and macroevolution in Jablonski etal. 1996.

Jablonski, D., D. H. Erwin, and J. H. Lipps, eds. 1996. Evolu-tionary paleobiology. University of Chicago Press, Chicago.

Kerr, S. R., and L. M. Dickie. 2001. The biomass spectrum: apredator-prey theory of aquatic production. Columbia Uni-versity Press, New York.

Kidwell, S. M. 2001. Preservation of species abundance in ma-rine death assemblages. Science 294:1091–1094.

———. 2002. Time-averaged molluscan death assemblages: pa-limpsests of richness, snapshots of abundance. Geology 30:803–806.

Lupia, R., S. Lidgard, and P. R. Crane. 1999. Comparing paly-nological abundance and diversity: implications for biotic re-placement during the Cretaceous angiosperm radiation. Pa-leobiology 25:305–340.

Miller, A. I. 1998. Biotic transitions in global marine diversity.Science 281:1157–1160.

Miller, A. I., and S. R. Connolly. 2001. Substrate affinities ofhigher taxa and the Ordovician Radiation. Paleobiology 27:768–778.

Miller, A. I., and M. Foote. 1996. Calibrating the Ordovician Ra-diation of marine life: implications for Phanerozoic diversitytrends. Paleobiology 22:304–309.

Miller, A. I., and J. J. Sepkoski. 1988. Modeling bivalve diversi-fication: the effect of interaction on a macroevolutionary sys-tem. Paleobiology 14:364–369.

Miller, A. I., S. M. Holland, M. L. Droser, and M. E. Patzkowsky.1998. Dynamics of the Ordovician Radiation: a comment onWestrop and Adrain. Paleobiology 24:524–528.

Novack-Gottshall, P. M. 2007. Using a theoretical ecospace toquantify the ecological diversity of Paleozoic and modern ma-rine biotas. Paleobiology 33:274–295.

———. 2008a. Ecosystem-wide body size trends in Cambrian-Devonian marine invertebrate lineages. Paleobiology 34:210–228.

———. 2008b. Using simple body size metrics to estimate fossilbody volume: empirical validation using diverse Paleozoic in-vertebrates. Palaios 23:163–173.

Novack-Gottshall, P. M., and A. I. Miller. 2003. Comparative tax-onomic richness and abundance of Late Ordovician gastro-pods and bivalves in mollusc-rich strata of the CincinnatiArch. Palaios 18:559–571.

Patzkowsky, M. E., and S. M. Holland. 1999. Biofacies replace-ment in a sequence stratigraphic framework: Middle and Up-per Ordovician of the Nashville Dome, Tennessee, USA. Pa-laios 14:301–323.

Patzkowsky, M. E., L. M. Slupik, M. A. Arthur, R. D. Pancost,and K. H. Freeman. 1997. Late Middle Ordovician environ-

mental change and extinction: harbinger of the end-Ordovi-cian or continuation of Cambrian patterns? Geology 25:911–914.

Payne, J. L., and S. Finnegan. 2006. Controls on marine animalbiomass through geological time. Geobiology 4:1–10.

Peters, S. E. 2004. Relative abundance of Sepkoski’s evolutionaryfaunas in Cambrian-Ordovician deep subtidal environmentsin North America. Paleobiology 30:543–560.

———. 2006. Genus richness in Cambrian-Ordovician benthicmarine communities in North America. Palaios 21:580–587.

Pope, M., and J. F. Read. 1995. Sequences and meter-scale cy-clicity of Middle to Late Ordovician cool water carbonatesand clastics of Kentucky. Pacific Section SEPM Field TripGuidebook 77:333–336.

Pope, M. C., and J. B. Steffen. 2003. Widespread, prolonged lateMiddle to Late Ordovician upwelling in North America: aproxy record of glaciation? Geology 31:656–656.

Ross, C. A., and J. R. P. Ross. 1995. North American depositionalsequences and correlations. Pp. 309–313 in J. D. Cooper, M. L.Droser, and S. C. Finney, eds. Ordovician odyssey. Short pa-pers for the Seventh International Symposium on the Ordo-vician System. Pacific Section SEPM, Fullerton, Calif.

Ross, R. J., and F. C. Shaw. 1972. Distribution of the Middle Or-dovician Copenhagen Formation and its trilobites in Nevada.U.S. Geological Survey Professional Paper 749.

Ross, R. J., Jr., T. B. Nolan, and A. G. Harris. 1980. The UpperOrdovician and Silurian Hanson Creek Formation of centralNevada. U.S. Geological Survey Professional Paper 1126-C.

Ross, R. J., Jr., N. P. James, L. F. Hintze, and F. G. Poole. 1989.Architecture and evolution of a Whiterockian (early MiddleOrdovician) carbonate platform, Basin Ranges of westernU.S.A. In P. D. Crevallo, J.L. Wilson, J. F. Sarg, and J .F. Read,eds. Controls on carbonate platform and basin development.SEPM Special Publication 44:167–185.

Ross, R. J., Jr., L. F. Hintze, R. L. Ethington, J. F. Miller, M. E.Taylor, and J. E. Repetski. 1997. The Ibexian Series (Lower Or-dovician), a replacement for ‘‘Canadian Series’’ in NorthAmerican chronostratigraphy. U.S. Geological Survey Open-File Report 93–598.

Rudkin, D. M., G. A. Young, R. J. Elias, and E. P. Dobrzanski.2003. The world’s biggest trilobite; Isotelus rex new speciesfrom the Upper Ordovician of northern Manitoba, Canada.Journal of Paleontology 77:99–112.

Saltzman, M. R., and S. A. Young. 2005. Long-lived glaciation inthe Late Ordovician? Isotopic and sequence-stratigraphic ev-idence from western Laurentia. Geology 33:109–112.

Savage, V. M. 2004. Effects of body size and temperature on pop-ulation growth. American Naturalist 163:429–441.

Sepkoski, J. J., Jr. 1996. Competition in macroevolution; the dou-ble wedge revisited. Pp. 211–255 in Jablonski et al. 1996.

———. 2002. A compendium of fossil marine animal genera.Bulletins of American Paleontology 363:560.

Sepkoski, J. J., Jr., and A. I. Miller. 1985. Evolutionary faunas andthe distribution of Paleozoic benthic communities in spaceand time. Pp. 153–190 in J. W. Valentine, ed. Phanerozoic di-versity patterns: profiles in macroevolution. Princeton Uni-versity Press, Princeton, N.J.

———. 1998. Analysing diversification through time. Trends inEcology and Evolution 13:158–159.

Sepkoski, J. J., Jr., and P. M. Sheehan. 1983. Diversification, fau-nal change, and community replacement during the Ordovi-cian radiations. Pp. 673–718 in M. J. S. Tevesz and P. L. McCall,eds. Biotic interactions in recent and fossil benthic commu-nities. Plenum, New York.

Sepkoski, J. J., Jr., F. K. McKinney, and S. Lidgard. 2000. Com-petitive displacement among post-Paleozoic cyclostome andcheilostome bryozoans. Paleobiology 26:7–18.

Shields, G. A., G. A. F. Carden, J. Veizer, T. Meidla, J. Y. Rong,


and R. Y. Li. 2003. Sr, C, and O isotope geochemistry of Or-dovician brachiopods: a major isotopic event around the Mid-dle-Late Ordovician transition. Geochimica Et CosmochimicaActa 67:2005–2025.

Springer, D. A. 1982. Community gradients in the MartinsburgFormation (Ordovician), southwestern Virginia. Ph.D. disser-tation. Virginia Polytechnic Institute and State University,Blacksburg.

Stanley, S. M. 1973. Explanation for Cope’s Rule. Evolution 27:1–26.

Stempien, J. A., R. A. Krause Jr., M. Kowalewski, A. I. Miller, andAnonymous. 2005. Brachiopod and bivalve size during theOrdovician; interpreting general trends. Geological Society ofAmerica Abstracts with Programs 37:14.

Titus, R. 1986. Fossil communities of the upper Trenton group(Ordovician) of New York State. Journal of Paleontology 60:805–824.

Titus, R., and B. Cameron. 1976. Fossil communities of the lowerTrenton Group (Middle Ordovician) of central and north-western New York State. Journal of Paleontology 50:12009–1225.

Valentine, J. W. 1973. Evolutionary paleoecology of the marinebiosphere. Prentice-Hall, Englewood Cliffs, N.J.

Vermeij, G. J. 2004. Nature: an economic history. Princeton Uni-versity Press, Princeton, N.J.

Webby, B. D., F. Paris, M. L. Droser, and I. G. Percival, eds. 2004.The Great Ordovician Biodiversification Event. ColumbiaUniversity Press, New York.

Westrop, S. R., and J. M. Adrain. 1998a. Trilobite alpha diversityand the reorganization of Ordovician benthic marine com-munities. Paleobiology 24:1–16.

———. 1998b. Trilobite diversity and the Ordovician Radiation:a reply to Miller et al. Paleobiology 24:529–533.

Westrop, S. R., L. A. Knox, and E. Landing. 1993. Lower Ordo-vician (Ibexian) trilobites from the Tribes Hill Formation, cen-tral Mohawk Valley, New York State. Canadian Journal ofEarth Sciences 30:1618–1633.

Westrop, S. R., J. V. Tremblay, and E. Landing. 1995. Decliningimportance of trilobites in Ordovician nearshore paleocom-munities: dilution or displacement? Palaios 10:75–79.

Wing, S. L., L. J. Hickey, and C. C. Swisher. 1993. Implicationsof an exceptional fossil flora for Late Cretaceous vegetation.Science 363:342–344.

Documents

Body size, energetics, and the Ordovician restructuring of ... · mixed carbonate-clastic depositional envi-ronments. 2. High stratigraphic resolution (single bed or small group of