Quantifying Seafood Through Time: Counting Calories in the Fossil Record

QUANTIFYING SEAFOOD THROUGH TIME: COUNTING CALORIES IN THE FOSSIL RECORD

SETH FINNEGAN

Department of Integrative Biology, University of California, Berkeley, 1005 Valley Life Sciences Building #3140, Berkeley, CA 94720-3140 USA

ABSTRACT.—Energy and nutrients are the fundamental currencies of ecology and changes in energy and nutrient availability are thought to have played an important role in the long-term development of marine ecosystems. However, meaningfully quantifying when, where, and how such changes have occurred has been a difficult and longstanding problem. Here, some of the various lines of evidence that have been brought to bear on this issue in the past two decades are reviewed, particularly those based on the fossil record of benthic invertebrates. This paper focuses on abundance, body size, and metabolism, three distinct but closely interrelated aspects of ecosystem structure that control (or are controlled by) energy fluxes. Each of these is subject to biases and inherent uncertainties that present significant challenges for making inferences from the fossil record, but when carefully controlling for environmental, taphonomic, and methodological variations there are robust trends that can be discerned above the noise. Integrating these different types of data in a single quantitative framework presents additional complications, but coherent patterns emerge from some such analyses. Accurate quantification of energetic trends in the fossil record is difficult but is a worthwhile goal because of its potential to illuminate the energetic dimension of major diversifications, extinctions, and secular ecological-evolutionary trends and link them more directly to their Earth Systems context.

INTRODUCTION conspicuous but poorly defined long-term trends in the ecological structure of marine fossil In 1993, Richard Bambach published a paper in assemblages. Equally importantly, they refocused Paleobiology entitled Seafood through time— the ongoing debate about Phanerozoic diversity changes in biomass, energetics, and productivity by reemphasizing the Earth Systems-focused in the marine ecosystem (Bambach, 1993). In this perspective of Valentine, Tappan, and others and subsequent papers (Bambach, 1993, 1999; (Valentine and Moores, 1970; Valentine, 1971, Bambach et al., 2002; Bambach and White, 2002; 1973; Tappan, 1982, 1986), and framing diversity Bush and Bambach, 2011), Bambach and trends in terms of the fundamental ecological colleagues assembled multiple lines of evidence currencies of energy and nutrients. to argue that: 1) the standing biomass and the Given the limitations of the available data at energy budgets of marine animal ecosystems had the time, Bambach’s arguments in 1993 were increased in steps over the course of the necessarily non-quantitative. He wrote that, Phanerozoic; 2) these steps had been facilitated by “While anecdotal and descriptive, the paper cites increases in marine primary productivity; and 3) unambiguous and robust patterns. On the global productivity increases were, in turn, linked to scale considered here, an effort at quantification expansions of terrestrial ecosystems via their would be too speculative at this time.” (Bambach, effects on continental weathering and nutrient 1993, p. 372). Two decades later, quantifying runoff. Along with papers and books by Geerat energetic trends remains a major challenge for Vermeij (1977, 1987, 1995, 2002, 2004) who also paleoecology, and the difficulty of this problem argued for stepwise increases in productivity and largely accounts for the fact that, although energetics, but thought that these increases were frequently cited, the hypotheses posed by related to volcanism and seafloor spreading Bambach and Vermeij have been tested only (Vermeij, 1995), these papers drew attention to rarely. In Ecosystem Paleobiology and Geobiology, The Paleontological Society Short Course, October 26, 2013. The Paleontological Society Papers, Volume 19, Andrew M. Bush, Sara B. Pruss, and Jonathan L. Payne (eds.). Copyright © 2013 The Paleontological Society. THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19

Over the past two decades, enormous distribution of marine biomass and associated quantities of data have been gathered and energy fluxes has changed throughout the assembled into databases. Interest in fossil Phanerozoic is important for several reasons. abundance patterns has grown, both for their Gradients in energy and nutrient availability play relevance to explicitly paleoecological questions a conspicuous role in controlling the distribution (McKinney et al., 1998; Lupia et al., 1999; Peters, of diversity and standing biomass in the modern 2004; Finnegan and Droser, 2005; Clapham et al., oceans (Rex et al., 2005, 2006; Belanger et al., 2006; Hull et al., 2011) and in recognition of the 2012), and have likely done so throughout Earth need to sample-standardize local (alpha) diversity history. Evolutionary events and trends may estimates (e.g., Adrain et al., 2000; Peters, 2006). ultimately be driven by physical forcings or Inclusion of quantitive abundance data in biological competition, but they are proximally occurrence-based databases such as the determined by the differential flow of energy and Paleobiology Database (Alroy et al., 2008) offers nutrients through individuals and populations a far richer picture of the fabric of the fossil (Van Valen, 1976). Changes in both marine and record than was available in 1993, especially terrestrial primary productivity have been when combined with stratigraphic databases hypothesized to be major factors in driving (Peters, 2005). There has also been a surge of Phanerozoic marine evolutionary and diversity interest in evolutionary body size trends, and trends (Tappan, 1982, 1986; Bambach, 1993, many size measurements of specimens from field 1999; Vermeij, 1995, 2002, 2004; Martin, 1996, censuses, museum collections, and published 2003; Falkowski et al., 2004) and are thought to monographs are now available (Kosnik, 2005; play an important role in several mass extinctions Payne, 2005; Hunt and Roy, 2006; Kosnik et al., (see van de Schootbrugge and Gollner, 2013; Hull 2006; Payne et al., 2009, 2012; Rego et al., 2012). and Darroch, 2013), but evolutionary patterns In neontology, the development of the cannot be confidently linked to productivity macroecological paradigm (Brown and Maurer, trends without information about the spatial and 1989; Brown, 1995; Witman and Roy, 2009) and environmental distribution of individuals and the Metabolic Theory of Ecology (MTE; Gillooly biomass through time. et al., 2001; Allen et al., 2002; Enquist et al., Similarly, direct or diffuse competitive 2003; Brown et al., 2004; Savage et al., 2004b) interactions have been invoked to explain the have spurred research focused on quantifying differential macroevolutionary success of clades energetic patterns across different taxa, through time (see discussion in Sepkoski, 1996), ecosystems, and scales. Spurred by concerns but, to the extent that they occur, such interactions about anthropogenic effects on marine ultimately are about the division of energy and ecosystems, marine ecological research has nutrient resources among individuals and greatly expanded knowledge of the metabolic populations. Consequently, putative cases of clade physiology and population ecology of extant competition cannot be properly evaluated without marine invertebrates (Brey, 2001). An ongoing data regarding the absolute (as opposed to renaissance in the development and application of relative) abundance, biomass, or metabolic stable isotope and other geochemical proxies has activity of the groups in question across also greatly refined our ability to reconstruct environments and through time (Finnegan and climate and environment in deep time. Droser, 2005, 2008). Summarizing this literature is beyond the scope of This paper discusses work, mostly from the this paper, but useful recent reviews include Ivany past two decades, that has sharpened and Huber (2012; various climate proxies), Katz understanding of the timing and magnitude of et al. (2010; various foraminiferan-based proxies), biomass and energetic trends. To limit the scope Schouten et al. (2013; lipid biomarkers), Brocks of the discussion, the focus herein is on the and Pearson (2005; deep-time biomarkers), Phanerozoic record of benthic invertebrates in Paytan (2009; paleoproductivity proxies) and level-bottom, shallow to deep subtidal platform Tribovillard et al. (2006; paleoproductivity and and shelf environments. These depositional paleoredox proxies). environments are by far the best represented in It is now feasible to at least outline a the stratigraphic record and, other than reefs, quantitative framework for examining energetic vents, and seeps, host the highest concentrations pattern in greater environmental and temporal of benthic macrofaunal biomass in the modern detail. Determining when, where, and how the oceans (Wei et al., 2010). Due to nutrient delivery

22 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS from continental runoff, shelf-marginal upwelling, sensitivity tests for evaluating trends in the fossil and the relatively high proportion of primary record and for comparing fossil estimates with productivity that is exported to the seafloor, these respiration data from modern benthic assemblages probably have been the most consistently are suggested. productive benthic marine environments throughout Earth history. In the modern ocean, BENTHIC ABUNDANCE AND BIOMASS these environments account for only 6% of the seafloor area, but contain an estimated 21% of As background for considering temporal trends, it global benthic biomass (Wei et al., 2012). is helpful to briefly discuss the geographic, Colonization of the deep sea (Smith and environmental, and bathymetric distribution of Stockley, 2005) or the development of planktonic benthic abundance and biomass in the modern pelagic ecosystems (Falkowski et al., 2004) are oceans. This reveals something about the physical not discussed herein. These represent enormous factors that exert the most influence on the expansions of global marine biomass, but the pre- distribution of individuals and biomass, and Mesozoic fossil record of deep sea macrofauna is therefore, which Earth systems changes might be fragmentary and poorly known, while pelagic expected to have had an influence on standing productivity trends are reviewed elsewhere in this stocks of abundance and biomass over geological volume (see van de Schootbrugge and Gollner, timescales. It also serves to highlight the range of 2013; Hull and Darroch, 2013). The goal of this values apparent in a single geological instant— paper is to review the evidence for long-term variation that must be taken into account when changes within a single (albeit very broadly attempting to delineate temporal trends. Wei et al. defined) habitat. (2010) added shallow-water (< 200 m) data to the This paper focuses on three types of evidence deep-sea benthic biomass and abundance dataset that are distinct but interrelated: abundance and compiled by Rex et al. (2006), and used a random biomass, body size, and metabolism. Following forest model trained on the relationship between Bambach (1993), long-term trends are the primary these data and a suite of physical predictors focus, although shorter-term patterns associated including depth, temperature, and various metrics with some mass extinctions are also reviewed. of primary production to predict the global Ways in which abundance, body size, and distribution of standing stocks of benthic metabolic data can be integrated utilizing simple abundance and biomass across four size classes. ecological and physiological principles to produce This analysis highlighted several important approximate estimates of individual, per-taxon, patterns. Whereas bacterial biomass exhibited and paleocommunity respiration rates are remarkably little variation with depth or latitude, discussed. The approach outlined herein is crude the standing biomass of invertebrate macrofauna in that it treats assemblages of fossils as directly and megafauna (individuals retained by a 520 µm comparable to living populations despite the well- mesh and larger, the size classes most commonly known distortions of population and community studied in the fossil record) decreased sharply structure introduced by taphonomy and time- with depth and distance from land and increased averaging. More sophisticated analyses that with latitude, exhibiting minima in the central account for other aspects of energy budgets such abyssal plains and maxima on mid- to high- as growth and reproduction and that integrate over latitude continental shelves (Fig. 1A, B). Controls the lifespan of an entire individual are possible on the global distribution of benthic invertebrate and have been attempted for some biomass are complex, but this and other analyses paleocommunities (Powell and Stanton, 1985), (Rex et al., 2006; Johnson et al., 2007; Ruhl et al., but require additional parameters that are difficult 2008; McClain et al., 2012; Wei et al., 2012) to estimate confidently for many extinct taxa. suggest that pelagic-benthic coupling can be Whether this approach is sufficient to discern strong and that important roles are played by: original environmental and temporal community 1) depth and its numerous physical correlates energetic gradients depends on the signal-to-noise because the proportion of net primary production ratio—the magnitude of the original gradients (NPP) that is exported to benthic ecosystems relative to the magnitude of the noise introduced decreases with depth (Lutz et al., 2007); 2) by the combined effects of taphonomic distortion primary productivity in surface waters, which and analytical simplification. Some of the major tends to influence the intercept but not the slope factors influencing this ratio are discussed, and of the depth-NPP export relationship; 3) distance

23 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19

FIGURE 1.—A–C) Global relationship between depth and: A) sampled biomass; B) abundance; and C) mean body size of benthic organisms in four size classes, modified from Wei et al. (2010). Relationships with latitude and longitude have been removed by partial regression. D–G) D) shows global bathymetry and the predicted geographic distribution of: E) biomass; F) abundance; and G) mean body size of invertebrate macrofauna + megafauna from a random forest model trained on the relationship between the samples in A–C and a suite of physical variables including depth, temperature, and primary productivity. D–G produced from Files S2 and S3 in Wei et al. (2010).

24 156 ANDREW B. SMITH AND A. J. MCGOWAN

TABLE 1. Numbers of maps with outcrop of given age that is fossiliferous (fossil) or unfossiliferous (barren) in each epoch. Peters Georef ϭ numbers of cited marine sedimentary formations that are fossiliferous or unfossilif- erous (from PetersFINNEGAN 2007: Fig.: QUANTIFICATION 2). A, Raw data. B,OF Data ENERGY corrected TRENDS for duration IN ANCIENT of epoch. ECOSYSTEMS Timescale from Gradstein et al. (2004).

Europe rock outcrop Australia rock outcrop Peters Georef from land because this tends to reduce nutrient diversity data alone. Although the data are scarce Fossil Barren % Barren Fossil Barren % Barren Fossil Barren % Barren delivery from both continental runoff and shelf- and often harder to quantify and interpret, there marginalA. Raw upwelling; data 4) latitude, possibly because are several direct lines of evidence for an overall of theCambrian comparatively short 74 food 52chains and 0.413 weak 77increase 32 in benthic0.294 10 biomass 16 through 0.615 the Ordovician 331 162 0.329 66 11 0.143 16 25 0.610 microbialSilurian loops at high 259 latitude (Kirchman 79 0.234 et al., 16Phanerozoic. 5 0.238 3 10 0.769 2009)Devonian and the effects 422 of water 83 temperature 0.164 on 56 18 0.243 14 27 0.659 microbialCarboniferous remineralization 308 rates, 232 the efficiency 0.430 of 32Unfossiliferous 16 0.333 versus fossiliferous 18 18 sediments 0.500 NPPPermian export to benthic 17habitats, and 19 the residence 0.528 56 A 19very coarse 0.253 measure 6 of the 13 spatiotemporal 0.684 Triassic 366 154 0.296 10 8 0.444 2 9 0.818 timeJurassic of organic carbon 2857 on the 370seafloor (Laws 0.115 et 19distribution 23 of 0.548fossil content 12 can be 7 obtained 0.368 by al.,Cretaceous 2000; Ruhl et al., 2511 2008). Hotspots 154 of elevated 0.058 265comparing 76 the 0.223 distributions 19 of fossiliferous 20 0.513 and macrofaunalPaleogene biomass 725 associated 56 with 0.072 many 40unfossiliferous 12 0.231 sedimentary 16 rocks. 2 Peters 0.111 (2007) submarineNeogene canyons (De 446 Leo et 39 al., 2010) 0.080 also 37and Peters 12 and 0.245 Heim (2010) 16 presented 7 evidence 0.304 reinforceB. Per million the importance year of terrigenous detrital for a long-term (although not obviously stepwise) inputs,Cambrian a point emphasized 1.48 by Bambach 1.04 (1993, 1.54Phanerozoic 0.64 decline in 0.20 the proportion 0.32 of 1999).Ordovician 6.37 3.12 1.27unfossiliferous 0.21 marine sedimentary 0.31 0.48 rocks. Peters Silurian 9.96 3.04 0.62 0.19 0.12 0.38 DevonianNotably, variation 6.70in the 1.32distribution of 0.89(2007) 0.29attributed this trend 0.22 to the prevalence 0.43 of at macrofaunalCarboniferous and megafaunal 4.81 biomass 3.63 appears to 0.50least episodically 0.25 hypoxic 0.28 conditions 0.28 in epeiric be Permian more strongly controlled 0.40 by 0.45 bathymetric 1.33depositional 0.45 environments, 0.14 which 0.31 were much (KaariainenTriassic and Bett, 8.51 2006) 3.58 and latitudinal 0.23more widespread 0.19 in the 0.05 Paleozoic 0.21 than in the Jurassic 46.08 5.97 0.31 0.37 0.19 0.11 (MoranCretaceous and Woods, 2012) 33.04 gradients 2.03 in mean body 3.49post-Paleozoic. 1.00 Smith and 0.25 McGowan 0.26 (2008) sizePaleogene (Fig. 1C,G) than 17.68 by gradients 1.37 in the 0.98observed 0.29 a similar trend 0.39 in Europe 0.05 (Fig. 2), but abundanceNeogene of individuals 18.58 (Fig. 1.63 1B,E,F), 1.54suggested 0.50 that the trend 0.67 instead 0.29 reflects an particularly in the shelf to slope environments that expanding biosphere in which the abundance of are best represented in the fossil record. Body size animals has gradually increased through time due patterns will be discussed in more detail after a to increases in primary productivity and nutrient review of the evidence for temporal trends in levels (Martin, 2003). The coarse bivariate biomass and abundance below.

Temporal trends in the fossil record Indirect evidence for a Phanerozoic increase in the standing biomass of benthic ecosystems from trends in diversity, paleocommunity structure, and ecospace filling has been reviewed most recently by Bush and Bambach (2011), and is only briefly summarized here. The diversity of skeletonized marine animals has increased substantially since the Cambrian both globally (Sepkoski, 2002; Alroy et al., 2008) and locally (Bambach, 1977; Bush et al., 2004, 2007)—a trend that implies a correlative increase in standing abundance and biomass. Proportions of predatory and motile genera also have risen sharply through time in multiple skeletonized groups, a trend that would be difficult to support energetically without commensurate increases either in primary productivity and the biomass of preyFIGURE species,1. A, or Number in prey of barren specificity marine units (Valentine, in each system/period (maps with rocks at outcrop in western Europe or Georef citations) per million years. B, Proportion of barren marine units per time interval. Georef ϭ sedimentary 1971)units or citation consumption survey (Peters efficiency 2007) and rock(Payne outcrop and data forFIGURE western 2.— EuropeProportions (this paper of marine Table 1). stratigraphic Linear regression units Finnegan,trend lines 2006) indicated of predators. with R2 of The 0.40 distribution and 0.45 respectively. of that Abbreviations: contain no Ca, recorded Cambrian; fossils. Cb, BlackCarboniferous; circles and Cr, taxaCretaceous; in ecospace D, Devonian; provides J, Jurassic; important N, Neogene; constraints O, Ordovician; regression Pe, Permian; lines based Pg, Paleogene; on a survey S, Silurian; of European T, Triassic. rock on biomass, but relationships between diversity units by Smith and McGowan (2008); gray diamonds and abundance patterns are extremely complex and regression line based on a GeoRef search by and poorly understood, and it is impossible to Peters (2007). Reproduced with permission from derive quantitative biomass estimates from Smith and McGowan (2008).

25 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19 binning scheme employed by these three studies is suggested by—among other things—trends in (fossiliferous vsersus unfossiliferous stratigraphic the thickness of preserved storm beds (Brandt, units) does not allow resolution of subtle trends in 1986; Sepkoski et al., 1991). fossil concentration, which would help to differentiate between these two models. The Absolute abundance: shell beds and bioclastic epeiric seaway hypothesis predicts that the fabrics abundance of fossils has remained relatively Fossil abundance data are critical for constant through time within different evaluating the ecological context of diversity depositional environments, and that the long-term trends (Peters, 2004; Clapham et al., 2006; Hull et decrease in the proportion of unfossiliferous units al., 2011) and for discerning trends in is explained by a decrease in the area of epeiric paleocommunity structure and function (Wagner seaways. In contrast, the expanding biosphere et al., 2006; Bush et al., 2007; Novack-Gottshall, hypothesis predicts that the abundance of fossils 2007), but most quantitative abundance counts are has approximately tracked global diversity trends collected without an accompanying measure of through time across a range of depositional the sediment volume processed (or, in the case of environments (Smith and McGowan, 2008). quadrat counts, the bedding-plane area censused). Differentiating between these two models, which Consequently, they can only measure the have very different implications for Phanerozoic abundances of different bioclast producers as a trends in paleocommunity energetics, should be proportion of the total count (relative abundance). facilitated by increasing integration of Normalizing abundance to the number of stratigraphic and paleobiological databases (e.g., individuals or fragments counted rather than to Heim and Peters, 2010; Peters and Heim, 2010; the amount of sediment processed forces the Finnegan et al., 2012). abundances of different groups to appear inversely correlated even if their absolute Bioturbation intensity abundance trajectories are entirely independent of Trends in the depth and extent of bioturbation one another (Fig. 3; Aitchison, 1982; Grayson, (ichnofabric) reflect infaunal activity through 1984; Finnegan and Droser, 2005). Thus, relative time. Ichnofabric development is influenced by abundance data are problematic because they can both abundance and per-capita activity level and create the impression of zero-sum competitive therefore cannot be interpreted solely in terms of ecological dynamics where none may have biomass density, but it is particularly valuable existed, and they cannot provide information because it is the only direct record of many about trends in the absolute abundance of fossils. nonskeletonized burrowing taxa (Thayer, 1983). Absolute abundance data are more difficult to Initial appearance of bioturbated sediments in the collect, especially in lithified sediments, and late Ediacaran–lower Cambrian (Seilacher and when available, they are difficult to interpret Einsele, 1982; Bottjer et al., 2000) was followed purely in terms of biological inputs. by increases in mean bioturbation intensity across Concentrations of skeletal material in marine a range of deposition environments during both sediments are determined by a complex interplay the Cambrian and Ordovician biodiversifications of numerous factors including biological (Droser and Bottjer, 1988, 1989, 1993; Mangano production and mortality rates, sedimentation and and Droser, 2004). In the wake of the Permo– reworking rates, and rates of dissolution and Triassic mass extinction, bioturbation was fragmentation (Kidwell, 1986; Kidwell et al., markedly reduced in many Early Triassic 1986; Davies et al., 1989). At the outcrop scale, depositional environments and did not return to bed-to-bed variations in bioclastic concentration pre-extinction levels until the Middle Triassic typically are controlled by processes such as event (Schubert and Bottjer, 1995; Pruss and Bottjer, burial, storm winnowing and reworking, 2004; Pruss et al., 2004). The subsequent condensation, dissolution, and bioturbation. This Mesozoic–Cenozoic diversification of burrowing physical overprinting adds considerable noise to taxa in several groups and the appearance of new the original signal of skeletal input. Even within a trace fossil types strongly imply a major increase relatively homogeneous sedimentary in bioturbation (Thayer, 1983; Vermeij, 1987). environment, the controls on local fossil There have been no field studies of long-term concentration can be complex and nonlinear Mesozoic–Cenozoic ichnofabric trends, but an (Finnegan and Droser, 2005; Tomašových and increase in bioturbation intensity over this interval Schlögl, 2008). Nevertheless, fossil concentration

26 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS L/M ORDOVICIAN DOMINANCE SHIFT 481

(Kucera and Malmgren 1998), and environ- activity over this interval were accompanied by mental change (Pandolfi 1999). substantially increased skeletal production rates. Abundance can be measured in two dis- This general trend is supported by point counts of tinctly different ways. Paleoecologists typical- thin sections and tabulations of bioclastic units in measured sections from Cambrian–Ordovician ly measure taxon abundance as a proportion strata in Utah and Newfoundland (Pruss et al., of all individuals in the sample (relative abun- 2010; Fig. 4), implying that it is a general trend at dance). The relative abundance structure of an least in Laurentian carbonate shelf and slope assemblage is, ideally, a probability distribu- environments. Fewer data are available to tion describing the likelihood that an individ- evaluate post-Ordovician trends in bioclastic ual randomly sampled from the assemblage abundance, but Kidwell and Brenchley (1994, will belong to the target group. There are both 1996) demonstrated that the proportional practical and theoretical reasons for this ap- frequency distribution of Jurassic shell beds is proach. Relative abundance data can be fairly more right-skewed (more thick beds) than that of easily collected in the field or laboratory, and Ordovician–Silurian shell beds, and that Neogene can be used to compare fossil assemblages shell beds tend to be considerably thicker than from widely varying depositional environ- Jurassic shell beds (Fig. 5). Known trends in ments. They are robust to variation in sample skeletal80 mineralogy and taphonomy (e.g.,PRUSS ET AL. PALAIOS size, especially where ecologically dominant taxa are concerned. The apportioning of in- dividuals among taxa (evenness, or its inverse, dominance) is essential information for cali- brating diversity estimates (Sanders 1968) and may itself be an ecologically important aspect of community structure (Magurran 1988; Pe- ters 2004a). Abundance can also be measured as a func- tion of the total area or volume sampled (den- FIGURE 1. Two hypothetical sets of absolute abundance sity, or absolute abundance), rather than the FtrajectoriesIGURE 3.— thatTwo produce hypotheticalidentical relative sets of abundance absolute number of individuals sampled. Absolute abundancetrends. In scenario trajectories 1, the that decline produce in relative identical abundance relative abundance data are routinely used by neon- abundanceof taxon A results trends. from In Scenario a true decrease 1, a decline in its absolute in the relativeabundance. abundance In scenario of taxon 2, the A declineresults isfrom an artifacta decrease of tologists to define ecological gradients. How- normalization and is driven by increases in the absolute in its absolute abundance. In Scenario 2, the decline is ever, paleontological absolute abundance data abundance of taxa B and C. an artifact of normalization and is driven by increases are harder to interpret than data from living in the absolute abundances of taxa B and C. assemblages. Fossil density distributions are Reproduced with permission from Finnegan and usually spatially and volumetrically patchy at Droser1982). (2005). Discounting the nonbiological factors several scales, and this patchiness reflects that affect fossil abundance, any change in the FIGURE 7—Principal Components Analysis of all unique formation-member- locality combinations. Four independent (but normalized) variables are shown: % taphonomic and depositional as well as eco- datarelative are abundance necessary of for a taxon constraining can be explained long-term Microbial carbonates, % Oolites, % Skeletal carbonates, and % Micritic carbonates. Labels show where pure micrite, skeletal limestone, oolite, and microbial carbonate logical patterns (Cummins et al. 1986a; Kid- changesin two ways in benthic (Fig. 1). biomass, A change and, in by its controlling absolute would occur (see Supplementary Data11 for sources used). well 1986; Miller and Cummins 1990). For this forabundance variations will in obviously sedimentary cause environment a correspond- and reason, and because they are difficult and time systematicallying change in censusing its relative and abundance. averaging Alter- across organisms increased in the Ordovician is a long-standing observation; many beds, it may be possible to extract a signal, however, quantification of the patterns presented here permits a more- consuming to obtain, paleontologists rarely natively, the shift may be driven by changes in focused evaluation of competing explanatory hypotheses. collect absolute abundance data (but see howeverthe absolute noisy, abundance of long-term of other trendstaxa in the skeletal as- Our data permit a test of the trends reported by Li and Droser (1997, Schneider 2001, for an example). productionsemblage, rate. such that the absolute abundance of 1999) for the Ibex area of Utah. The three data sets assembled here confirm a marked increase in shell-bed abundance in the Ibex region; Although only a handful of such studies have FIGUREIGURE 6—Proportions of stratigraphic units (formations or members) logged as Nevertheless, there are compelling reasons the taxon itself does not change, but its relative Fskeletal limestone 4.— (fossilProportions wackestones, packstones, of or stratigraphic grainstones), plotted against units age furthermore, our data (despite differing taphonomic biases) reveal that for collecting these data in some situations. It beencontribution conducted, to theythe sa havemple been necessarily informative. does. Li (formationsin measured sections or from members) A) Newfoundland logged (S. Pruss, as field skeletal notes, 2005–20 limestone06) and B) the proportional abundance of identifiable skeletons in carbonate rocks and Droser (1997, 1999) demonstrated that the (fossilUtah (compiled wackestones, from S. Finnegan field packstones, notes, 2000–2005, and or from grainstones), Hintze, 1973); S3 increased across facies and, indeed, throughout Laurentia. Thus, all is impossible to resolve the ecological mean- This has been referred to as ‘‘the problem of 5 Series 3; Dap. 5 Dapingian; Dar. 5 Darriwilian. frequency and the mean thickness of shell beds in plotted against age in measured sections from A) observations point toward the same conclusion (see Supplementary ing of abundance trends on the basis of rela- closed arrays’’ (Grayson 1984). Discriminating Data1; Fig. 7). For comparison, skeletons can account for 90% of total carbonates of the Basin and Range region of the NewfoundlandFurongian Cambrian (S. sectionsPruss, andfield Middle notes, to 2005–2006); Upper Ordovician B) tive abundance data alone (Jackson 1997). between the two cases is of obvious signifi- western US increased through the Cambrian and westernsections compriseUtah (S. essentially Finnegan non-overlapping field notes, groupings, 2000–2005, with Lower and Normalizing to the number of individuals in acrosscance: thein the Early–Middle former case Ordovician the shift in boundary, relative fromOrdovician Hintze, sections 1973); spanning S3 = the Series full range 3; Dap. (Fig. 7).= Dapingian; Skeleton-rich limestones formed in later Cambrian seaways, but Cambrian sections the sample necessarily couples variables that suggestingabundance that has increases true ecological in diversity significance and infaunal for Dar. = Darriwilian. Reproduced with permission from Prussare dominated et al. (2010). lithologically by micrites, oolites, and microbialites. In may be entirely uncorrelated (Aitchison 1981, the taxon under consideration; in the latter contrast, post-Tremadocian Ordovician sections are dominated by skeletal limestones.

27 DISCUSSION The late Cambrian–Early Ordovician interval stands out as distinctive against the broad background of Phanerozoic marine evolution. Skeletons, largely trilobite and echinoderm remains, make only a limited contribution to limestones of this age, with abundant ooids, microbialites, and micrites suggesting a carbonate factory dominated by physical and microbial processes. In particular, reef- forming metazoans were scarce for 40 myr following archaeocyathid extinction (Rowland and Shapiro, 2002), radiating again in the Middle Ordovician. Following this interval, a sharp global increase in the generic diversity of carbonate-secreting metazoans (Sepkoski, 2002; Webby et al., 2004; Peters, 2005a) (Fig. 8) and an increase in the depth and complexity of FIGURE 8—Generic diversity of calcifying animal groups from the Cambrian into bioturbation suggests rapid diversification and ecological transformation the Ordovician (Peters [2005a] database, using Sepkoski’s [2002] data). (Droser et al., 1996; Miller and Foote, 1996; Adrain et al., 1998; Webby et al., 2004). That the diversity and abundance of well-skeletonized 1 www.paleo.ku.edu/palaios Downloaded from geology.gsapubs.org on April 30, 2013

tributions of shell-bed thicknesses were then thick. For these, we tabulated the number of whelmed by the virtually uncountable and compared by using the nonparametric Kol- different kinds of shell beds <10 cm thick in identical very thin shell beds (e.g., storm mogorov-Smirnov test (Sokal and Rohlf, a given lithostratigraphic unit rather than beds, turbidites) that characterize some 1981). The onlyT exceptioHE PALEONTOLOGICALn to this system of tallyin SOCIETYg every exampl PAPERSe of eac, Vh kindOL.. 19This ap- units, as well as to minimize artifactual vari- data tabulation was for shell beds <10 cm proach was necessary so as not to be over- ation related to the number of outcrops that were available per stratigraphic unit; thicker shell beds can usually be identified uniquely 50 -ir Neogene n = 218 and traced confidently between outcrops, whereas very thin ones generally cannot and u> Calcific "S 40- thus might erroneously be counted more E2 Other epifaunal bivalves, bryozoans, than once. This procedure produces fre- echinoids, subordinate ostraceans CD quency distributions with a highly conserva- w 30- • Ostracean bivalves tive minimum value for the first size class. Aragonitic Statistical comparisons were performed by using both the full frequency distribution and one in which the first size category was omitted (p values denoted as full or trun- cated, respectively).

OBSERVED PATTERNS IN SHELL-BED THICKNESSES Neogene Neogene shell beds exhibit a broad range in thickness and taxonomic composition. Thin, decimetre-scale concentrations re- Jurassic n = 110 cording brief events such as storms, oppor- tunistic settlement, and predation are dom- Calcific inant (i.e., define the mode), but shell beds • All brachiopods >50 cm thick are very common (Fig. 1). • Ostracean bivalves Aside from submarine debris flows, these thicker examples are internally stratified or Aragonitic thoroughly amalgamated accumulations • Infaunal or mixed life habits, primarily mollusks built by multiple short-term events of re- working and recolonization; they include bioclastic tidal ridges, washover fans, and condensed transgressive facies (e.g., Kid- well, 1991). The frequency distribution does VZZ\ 777, not vary significantly with tectonic setting (full p > 0.30, truncated p > 0.50) or for field vs. literature sources of data (full p > 0.50, truncated p > 0.20); however, midlati- tude records, which dominate the Neogene Ordovician-Silurian n = 85 data set, might contain significantly more thin shell beds than do low-latitude records Calcitic (full p < 0.10, but truncated p < 0.005) • Other calcitic brachiopods (Fig. 21). H Pentamerid brachiopods Benthic bivalves are the most common El Trilobltes dominant bioclast in Neogene shell beds • Trepostome bryozoans across the full range of thicknesses. Com- Aragonitic positions vary from entirely epifaunal and t Trimerellacean brachiopods calcitic (pycnodont and ostreid oysters, pec- • Archaeogastropods tinids, anomiids) to dominantly infaunal and aragonitic (especially mono- and polytaxic bivalve assemblages of arcids, glycymerids, isognomids, chamids, astartids, crassatellids, mactrids, venerids, and corbulids). No single 0.5 0.6 0.7 0.8 0.9 1 1.5 group or life habit is responsible for the tail Thickness (m)

FIGURE 5.—PhanerozoicFigure trend1. Frequenc in y the distribution thicknesss of thicknes frequencys of bioclast-supporte distributiond andshell bedtaxonomics (bioclast s composition> 2 1GSA Dat ofa shellRepositor beds,y item 9452, Table 1, reproduced with permissionmm, excludin fromg crinoids) Kidwell, showin andg Brenchley significant shif (1994).t to right-skewed distributions over time. Pattern of Data Collection and lists of data Where thicknesses fell at boundary, shell beds were tallied in larger size class. Contrast be- sources, is available on request from Docu- tween Ordovician-Silurian and Neogene data sets reflects evolution of several bioclast- ments Secretary, GSA, P.O. Box 9140, Boulder, producing groups and does not depend upon single biomineral or life habit. CO 80301. Kowalewski et al., 1998; Oji et al., 2003) cannot sections from a late Permian–Early Triassic easily explain this1140 trend; hence, the most carbonate platform, Payne et al. (2006) showedGEOLOGY , December 1994 parsimonious explanation is a combination of that multiple facies record order-of magnitude increased durability and increased skeletal declines in the volumetric contribution of animal production rates (Kidwell and Brenchley, 1994, bioclasts across the Permian–Triassic (P–T) 1996). boundary. Animal bioclastic contributions to Clear changes in bioclast abundance are also carbonate production remained low throughout associated with at least some major mass the Early Triassic, and had not fully returned to extinction events (see also van de Schootbrugge pre-extinction levels even by the early Middle and Gollner, 2013; Hull and Darroch, 2013). In a Triassic (Payne et al., 2006). Taken together with study of more than 600 hand samples and thin the similar Permian–Triassic trend in bioturbation

28 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS intensity (Schubert and Bottjer, 1995; Pruss and Latitudinal gradients in mean individual size have Bottjer, 2004; Pruss et al., 2004), the decrease also been recognized, but are less pronounced implies that the benthic biomass of animals was (Fig 1C, G) and their causes less well understood. very low for a substantial period of time Despite much study of interspecific body-size following the extinction. gradients within marine invertebrate groups (Roy The Early Triassic example highlights another et al., 2000; Roy, 2002; McClain, 2004; important strength of biomass data. Diversity may Kaariainen and Bett, 2006; McClain et al., 2006; take millions of years to fully recover following a Berke et al., 2013) broadly generalizable major mass extinction simply because origination macroecological patterns of interspecific size of new taxa takes considerable time—a lag does variation are not apparent (Berke et al., 2013), not necessarily imply ongoing environmental implying that mean size trends primarily reflect disruption (Kirchner and Weil, 2000; but see Lu et intraspecific size clines and changes in species- al., 2006). However, on geological timescales, abundance structure rather than interspecific size benthic biomass should respond essentially trends. instantaneously to changes in energy and nutrient Regardless of the mechanisms that give rise availability. Indeed, the relatively few benthic to body-size gradients, body size is a crucial taxa that do proliferate in the Early Triassic are parameter for any consideration of long-term mainly generalist ‘disaster’ taxa (Schubert and trends in ecosystem energetics because it is Bottjer, 1995; Rodland and Bottjer, 2001). Given strongly correlated with individual metabolic rate this, the protracted interval of low bioclastic (Gillooly et al., 2001; West, 2002; Glazier, 2005; abundance implies either that primary production Seibel and Drazen, 2007; see discussion below). was generally low or that other environmental Trophic level is also closely related to individual conditions prevented animal populations from body size in marine ecosystems (Jennings et al., fully exploiting available nutrient and energy 2001; Kerr et al., 2001; Shurin et al., 2006), but resources (Payne et al., 2004, 2006; Ramezani et due to the enormous ontogenetic size range al., 2006; Sun et al., 2012). Comparable studies of spanned by most marine benthic species, there other major mass extinction events are needed to may be only a weak relationship between mean determine the degree to which benthic biomass adult body size and trophic level (Jennings et al., trends track trends in diversity or in 2001; Shurin et al., 2006), particularly given that environmental proxy data across different the majority of benthic invertebrate species are depositional environments and through time (see suspension or deposit feeders. Hull et al., 2011; Hull and Darroch, 2013, for Because individual metabolic rate scales pelagic examples). positively with body size, body size also constrains population density and local abundance BODY SIZE AND BODY MASS (Damuth, 1991; Kerr et al., 2001; Marquet et al., 2005). On average, big animals tend to be less The data summarized above imply a long-term common than small animals, although the form of increase in benthic biomass, although they offer this relationship and its dependence on sampling, only the coarsest outline of timing and magnitude spatial scale, environment, and taxonomic group of increase. Thus far, this review has treated is controversial, and it may not always be biomass and absolute abundance in the fossil apparent in local benthic communities (Warwick record as largely synonymous, but the biomass of and Clarke, 1996; Dinmore and Jennings, 2004). a given taxon per unit area is a function of both its In principle, it is possible for an overall population density and its mean body size. As Phanerozoic increase in absolute abundance to previously noted, global-scale gradients in the have been offset by compensatory reductions in modern distribution of benthic macrofaunal mean body size such that total benthic energy biomass largely reflect the influence of mean size budgets were unchanged. However, Phanerozoic rather than of abundance (Fig. 1). Broad trends in body size distribution (Kosnik et al., bathymetric gradients in mean individual size 2011) provide little support for this hypothesis. have been recognized for some time, and are Renewed interest in the evolutionary and thought to be related to decrease in the ecological meaning of body size over the past availability of energy and nutrients from surface decade has greatly increased the amount and the productivity with increasing depth and distance phylogenetic diversity of available fossil body- from productive coastal waters (Rex et al., 2006). size data. Although there is much variation in how

29 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19 body size is measured in the literature, different 7). This dataset is particularly relevant to size metrics tend to be very strongly correlated energetic considerations because the included with one another and even simple, one- genera cumulatively account for a dimensional size metrics capture most variation disproportionate percentage (≧ 40%) of the (Kosnik et al., 2006; Novack-Gottshall, 2008a). A recorded occurrences of these clades in each of 48 full review of the current state of knowledge of Phanerozoic time intervals (Kosnik et al., 2011). body size trends in marine invertebrate groups Where they overlap, the data sets of Kosnik et al. would run to many pages and is beyond the scope (2011) and Novack-Gottshall (2008b) show of this paper, but some general trends can be generally similar trends. Brachiopods increased in highlighted. mean size by roughly an order of magnitude through the early to mid-Paleozoic, then exhibited Maximum size of marine animals relative stasis thereafter. The mean size of The maximum known size of marine animals bivalves increased slightly in the Cambrian– has increased by about three orders of magnitude Ordovician, and showed no secular trend from the lower Cambrian to the Recent (Payne et thereafter, although there is some indication of a al., 2009). Most of this increase occurred during muted Late Triassic–Early Cretaceous maximum. the early Paleozoic, although within-clade Gastropods increased slightly in mean size maximum size trajectories show considerable through the Ordovician, declined slightly from the variation (Payne et al., 2009). Maximum size is a Silurian through the Triassic, and then increased useful measure of evolutionary potential (Bonner, slightly but rapidly in the mid-Jurassic, followed 2006), and may provide information about by relative stasis to the Recent. Chordates were environmental boundary conditions such as not included in the Novack-Gottshall (2008b) or oxygen availability (Cloud, 1972), a potential Kosnik et al. (2011) analyses, but Albert and explanation for the early Paleozoic increase in Johnson (2012) recently examined the fossil maximum size (Payne et al., 2009, 2011; Dahl et record of fish, and found that their mean size al., 2010; but see Butterfield, 2011). In principle, increased substantially during the Cambrian– maximum size is also constrained by primary Silurian and then did not change substantially productivity and the length and complexity of thereafter. food chains (Kerr et al., 2001), but the As with bioclastic content and bioturbation relationship between productivity and maximum trends, there are relatively short-term decreases in size is not well understood. For making inferences mean body size associated with at least some of about productivity and energy availability, the major mass extinction events (see Hull and measures of variance and central tendency are Darroch, 2013). The generality of this so-called more informative, especially when combined with ‘Lilliput effect’ (Urbanek, 1993) is disputed, but relative or absolute abundance data (Rex et al., the pattern appears robust for some groups during 2006; Finnegan et al., 2011; McClain et al., 2012) or after the Permian–Triassic (Fraiser and Bottjer, 2004; Payne, 2005; He et al., 2007; Twitchett, Size trends within clades 2007; Rego et al., 2012; but see Brayard et al., Novack-Gottshall (2008b) gathered size data 2010) and Cretaceous–Paleogene (Aberhan et al., from taxonomic monographs for genera occurring 2007) extinctions. The ecological-evolutionary in deep subtidal level-bottom assemblages from meaning of the Lilliput Effect is controversial the Cambrian through the Devonian, and found an because there are several distinctly different ways increase in mean genus size within several (but in which such a pattern could arise (Harries and not all) taxa through this interval (Fig. 6), a trend Knorr, 2009; Rego et al., 2012). The fact that explained by primarily by increased three- many of the foraminiferan genera that survived dimensionality (i.e., ‘fattening’ rather than the late Permian mass extinction experienced increasing area). Kosnik et al. (2011) compiled mean size reductions in the Early Triassic (Rego data on the body sizes of 933 of the most et al., 2012) suggests that the post-extinction commonly occurring brachiopod, gastropod, and interval was characterized by environmental bivalve genera in the Paleobiology Database (Fig. conditions conducive to small size, but whether

FIGURE 6.—Cambrian–Devonian trends in the mean estimated body volume of genera occurring in deep subtidal soft-substrate fossil assemblages, reproduced with permission from Novack-Gottshall (2008b). →

30 222 FINNEGAN: QUANTIFICATIONPHILIP M. OF NOVACK-GOTTSHALL ENERGY TRENDS IN ANCIENT ECOSYSTEMS

FIGURE 5. Cambrian–Devonian trends in mean body volume of eight common classes in deep-subtidal, soft-sub- strate assemblages. Plot details are the same as in Figure 1. 31 THEPHANEROZOIC PALEONTOLOGICAL DURABILITY SOCIETY CHANGES PAPERS, VOL. 19 313

FIGURE 5. Occurrence-weighted shell size by taxonomic group. Phanerozoic timescale on the x-axis as in Figure 2. FGeometricIGURE 7.— meanOccurrence-weighted of x and y on the y-axisPhanerozoic in millimeters trends with in the a log shell2 scale. sizes In of the the left most column common (A–C), brachiopod,the solid black bivalve, line is anda three-point gastropod (three-bin) genera. Y movingaxis shows average geometric of the mean mean occurrence-weighte of length and widthd shellin millimeters size. The gray on a area log2 is scale. bounded In the by left the column5th and (A–C), 95th quantiles, the solid which black are line used is as a three-point proxies of the (three-bin) smallest and moving larges averaget occurring of the shell mean sizes. occurrence-weighted In the right column shell(D–F) size. are theGray mean, area 5th,is bounded and 95th by quantiles the 5th andas fit 95 byth PaleoTSquantiles,(heavy which black are lines);used as each proxies genus of is the plotted smallest with and a circle largest the occurringsize of which shell is sizes. proportional In the right to its column relative (D–F) occurrence are the in themean, time 5th bin., and Th 95e threeth quantiles groups (heavy show distinctblack lines); and independent each genus histories of change in shell size. is plotted with a circle the size of which is proportional to its relative occurrence in the time bin. Reproduced with permission from Kosnik et al. (2011). support (Table 2). The support for a direc- bins are removed a model of stasis is thistional was trenda consequence is found of low entirely productivity, within high the overwhelminglySkeletal size versus favored. wet mass The and increase ash-free dry in temperature,Cambrian–Ordovician low oxygen levels, when low pH,brachiopods or some shellmass size through the Cambrian–Ordovician combinationmore than of double these factors in size is not from yet known.,8 mm to is also Paleontologists seen in largest often occurringuse skeletal shells dimensions (the .16 mm (Fig. 5A,D). Once the Silurian shell 95thto estimate quantile). body Maximum volume; however, size remains it is high mass size is achieved it remains essentially un- (,rather45 mm)than volume through (specifically, the remainder the total ofmass the of changed through the remainder of the Phan- Paleozoic, but decreases slightly to ,35 mm erozoic, and if the Cambro-Ordovician time in the Meso-Cenozoic coincident with the 32 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS proteins, lipids, and carbohydrates; i.e., organic (rhychonelliform) brachiopods, two of the taxa mass), that has the greatest influence on that commonly numerically dominate Paleozoic individual metabolic rate and energy content. assemblages, have very low AFDM/WM ratios Within a given group, there typically is a tight relative to Cenozoic dominants such as allometric relationship between skeletal gastropods, bivalves, and decapods. In the case of dimensions and body mass, and the former can be crinoids, the reported AFDM/WM ratio may still treated as a direct proxy for the latter. It is often be an overestimate for most Paleozoic taxa desirable to make biomass comparisons among because data are primarily based on different groups, however, and in this case there measurements of comatulids, which have high are other parameters that must be estimated. AFDM/WM relative to stalked crinoids For example, the Phanerozoic transition from (Baumiller and Labarbera, 1989). In the case of generally brachiopod-dominated to bivalve- brachiopod versus bivalve, combining DM/cm3 dominated paleocommunities is one of the most estimates from Peck (1993) and AFDM/DM striking and studied paleoecological trends in the estimates from Brey (2001) suggests that bivalves fossil record (Gould and Calloway, 1980; Thayer, typically have from 3 to 73 times the organic 1983, 1986; Rhodes and Thompson, 1993; mass of brachiopods with equivalent skeletal Clapham et al., 2006; Clapham and Bottjer, 2007), volumes. and one that has important implications for benthic energetic trends (Bambach, 1993). As has METABOLISM been pointed out by Peck (1992, 1993), rhychonelliform brachiopods are small animals Brey (2001) also compiled more than 20,000 occupying relatively voluminous shells, and the measurements of resting metabolic rate density of living tissue in rhychonelliform (respiration) for aquatic invertebrates. Plotting brachiopods commonly is an order of magnitude metabolic rate against body mass (AFDM) (or more) less than that of bivalves (Peck, 1992, illustrates that both body size and ambient 1993). To directly compare brachiopod and temperature are strongly positively correlated bivalve biomass therefore requires different with individual resting metabolic rate (energy models of the relationship between shell size and *mass-1* time-1) across phylogenetically, body mass for these two groups. Equations ecologically, and ontogenetically disparate relating shell size to soft tissue mass have been individuals (Fig. 9). Whether size constrains determined for gastropods and bivalves by Powell individual metabolic rate or, as has been and Stanton (1985) and for brachiopods and suggested, vice versa (Pauly, 2010), this bivalves by Peck (1993). observation is important for analyses of energetic Because fresh tissues contain large amounts trends in the fossil record because it suggests that, of water, individuals are often weighed both especially if temperature variation is reduced by before and after drying to determine wet mass controlling for depth and latitude (or by direct (WM) and dry mass (DM). Dry mass includes a proxy measurements), body size measurements variable amount of mineral content, so organic will capture most of the variation in individual mass is usually measured as ash-free dry mass metabolic rates within and between fossil (AFDM), which is DM minus the mass of the assemblages (Powell and Stanton, 1985, 1996; residuum left over following combustion in a Cummins et al., 1986; Finnegan and Droser, muffle furnace or bomb calorimeter. This 2008; Finnegan et al., 2011). procedure also yields the energy content of the The mass dependence of individual metabolic individual, usually given as J/mg AFDM. rate typically is expressed by an equation of the Nearly 6000 energy content measurements, form: representing ~3500 species, have been compiled by Brey (2001). Mean ratios of ash-free dry mass (Eq. 1) to wet mass (AFDM/WM) and energy yield (J/ mg AFDM) from this database are plotted for where B = individual metabolic rate, M = body sixteen paleontologically important groups in mass, B is an empirically fit taxon-specific Figure 8. Although there is little variation in mean 0 normalization constant, and b is a scaling J/mg AFDM across these taxa, there is coefficient that typically falls in the 2/3 to 1 range considerable variation in AFDM/WM (Brey et al., and commonly is very close to 3/4. The 1988). It is notable that crinoids and articulate

33 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19

AFDM/WM AFDM/WM J / mgAFDMJ / mgAFDM Anthozoa Anthozoa Anthozoa Anthozoa

Articulata Articulata Articulata Articulata

Asteroidea Asteroidea Asteroidea Asteroidea

Bivalvia Bivalvia Bivalvia Bivalvia

Cephalopoda Cephalopoda Cephalopoda Cephalopoda

Cirripedia Cirripedia Cirripedia Cirripedia

Crinoidea Crinoidea Crinoidea Crinoidea # log10(N)measurements log10(N) 2.0100 2.0 Decapoda Decapoda Decapoda Decapoda 30 1.5 1.5 Demospongiae Demospongiae Demospongiae Demospongiae 10 1.0 1.0 3 Echinoidea Echinoidea Echinoidea Echinoidea 0.5 1 0.5 Gastropoda Gastropoda Gastropoda Gastropoda

Gymnolaemata Gymnolaemata Gymnolaemata Gymnolaemata

Holothuroidea Holothuroidea Holothuroidea Holothuroidea

Ophiuroidea Ophiuroidea Ophiuroidea Ophiuroidea

Ostracoda Ostracoda Ostracoda Ostracoda

Polychaeta Polychaeta Polychaeta Polychaeta

0.0 0.1 0.0 0.2 0.1 0.2 0 10 0 20 10 20

FIGURE 8.—Ash-free dry mass to wet mass ratios (AFDM/WM) and energy yields per unit ash-free dry mass (J/ mg AFDM) from Brey’s (2001) database. Bars indicate means and error bars indicate 95% confidence intervals. Shading of bars indicates the number of measurements for each taxon. temperature dependence of B in this formulation biochemical reaction rates (West et al., 1997; is traditionally expressed by inclusion of a Q10 Gillooly et al., 2001; Savage et al., 2004a): term. For any value of b < 1, respiration rate per unit mass scales as a negative function of body (Eq. 2) mass (e.g., if b is 3/4, respiration rate per unit mass scales as m-1/4), so that large organisms where T = temperature in ° K, B is an empirically require less energy per unit mass for respiration 0 fit taxon-specific normalization constant, E is the than do small organisms. The generality of 1/4 average activation energy of rate-limiting power scaling in ecology and physiology and the biochemical reactions, and k is Boltzmann’s potential mechanisms underlying these constant. Although this model is highly relationships have been the subject of intense controversial, it provides a useful framework for debate over the past several years (e.g., West et considering metabolic rates in the fossil record, al., 2003; Brown et al., 2004; Savage et al., and, for most paleoecological applications, very 2004b, 2008; Glazier, 2005, 2010; Seibel and similar trends are obtained whether the MTE or a Drazen, 2007; White et al., 2007; Price et al., more traditional Q formulation is used. Most 2012). The metabolic theory of ecology (MTE; 10 empirically determined Q formulations are close Gillooly et al., 2001; Allen et al., 2002; Savage et 10 to 2, so that whether using the MTE or Q al., 2004a) posits that 3/4-power scaling of 10 formulation, the effect of a 10 °C increase in individual metabolic rate with body size is a ambient temperature on individual metabolic rate universal feature of multicellular life that arise is approximately equivalent to that of a ~75% from the fractal nature of fluid distributary increase in body mass (Fig. 10). The networks. The MTE reformulates Eq. 1 in paleontological examples that are summarized explicitly thermodynamic terms to model the below employ the MTE model and assume a b of temperature-dependence of metabolic

34 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS

FIGURE 9.—Measurements of respiration plotted against body mass for all taxa (top left panel) and taxa that are at least partially skeletonized and/or paleontologically important (remaining panels). The temperature at which respiration was measured is indicated by the color scale. Although Brey (2001) reports body mass in energetic units (J), body masses are here plotted as g AFDM assuming a uniform conversion factor of 2.1 * 104 J / g AFDM (Fig. 7). The exceptionally large mass ranges exhibited by some taxa reflect inclusion of larval stages.

3/4, but this is not necessarily appropriate for all effects of body mass, temperature, depth, diet, and marine invertebrates under all conditions (Glazier, a host of other potential predictors on mass- 2005, 2006; Seibel, 2007). Derivations of b and specific metabolic rate. Predicted metabolic rates B0 for various marine invertebrate groups can be at a fixed body mass and temperature show found in numerous references, including considerable variation among the Vladimirova (2001), Vladimirova et al. (2003), paleontologically important taxa included in Glazier (2005), Seibel (2007), and Makarieva et Brey’s (2001) database (Fig. 11), with al. (2008), or can be extracted from Brey’s (2001) echinoderms generally having the lowest compilation. predicted metabolic rates, and mollusks, As an alternative to linear models, Brey particularly bivalves and cephalopods, having the (2010) used a neural net model to model the highest predicted metabolic rates. This model

35 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19

8 4 energy requirements. Basal metabolic rate measurements are made with the explicit goal of 3 factoring out organismal behavior and activity 2 4 level, but one of the most striking features of the 1 benthic fossil record is a Phanerozoic increase in

0 the proportion of at least facultatively motile species and individuals (Bush and Bambach, -1 0 2004, 2011; Bush et al., 2007). In addition, as has -2 been emphasized by Bambach (1993, 1996), Body Mass (g) Body Vermeij (1987, 2004), Thayer (1983) and others,

10 -3 -4 relative activity levels and power (sensu Vermeij, Log -4 2004) have likely increased even among motile -5 taxa. Active metabolic rates are difficult to -6 measure for benthic invertebrates and difficult to generalize to the ecosystem scale or integrate over -8 0 10 20 30 40 organismal lifespans. Consequently, it is not easy Temperature, °C to quantitatively estimate the energetic significance of Phanerozoic trends in motility and FIGURE 10.—The relative effects of temperature and activity level. However, given that active and body mass on the log10 basal metabolic rate of a hypothetical individual according to the predictions of resting metabolic rates can differ quite the metabolic theory of ecology (MTE). Mass range substantially in some species (Seibel, 2007), and reflects the full range of marine metazoan body size may scale differently with body size (Nagy, (Bonner, 2006) and temperature range includes the 2005), the effect may be large. biologically relevant range experienced by the vast majority of marine organisms. Contours indicate lines Anthozoa of constant log10 basal metabolic rate (W). Q10-based formulations for the mass- and temperature- Articulata dependence of basal metabolic rate give similar results. Asteroidea Bivalvia (other) estimates that the resting metabolic rate of a Cephalopoda brachiopods is about half that of bivalves, a ratio Cirripedia that is comparable to previous estimates (but see Crinoidea Demospongiae Ballanti et al., 2012). Perhaps the most striking Echinoidea feature of these data is not the relative differences, Gastropoda (other) but rather the narrow, approximately fourfold Gymnolaemata range of variation seen among phylogenetically Heterodonta and ecologically disparate clades. These results Holothuroidea are consistent with other data suggesting that Inarticulata mass- and temperature-specific resting metabolic Malacostraca # measurementslog10(N) rates exhibit a very narrow range of variation Neogastropoda across 20 orders of magnitude in body mass, Ophiuroidea 31000 implying conservation of fundamental metabolic Ostracoda 2100 biochemistry across all metazoa (Makarieva et al., Polychaeta 2008). The narrow range of mass- and Polyplacophora 10 temperature-specific resting metabolic rates 0.0 0.2 0.4 0.6 0.8 means that, when estimating individual metabolic Respiration (J mg−1d−1) rates for fossil data, uncertainty regarding the conversion of skeletal size measurements to FIGURE 11.—Mass- and temperature-specific basal metabolic rate estimates (for an individual weighting 1 organic mass estimates (see above) often will be a gram at an ambient temperature of 20° C) predicted by much more important source of error than a neural net model formulated by Brey (2010). Bars uncertainty about the mass-specific metabolic indicate specific respiration rate and error bars indicate rates or the taxa in question. 95% confidence intervals. Shading of the bars A caveat is necessary concerning the use of indicates the number of measurements included in the basal metabolic rate as a proxy for metabolic training dataset.

36 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS

ENERGETICS: INTEGRATING through time or across environments is that it ABUNDANCE, BODY SIZE, AND requires: 1) determination of several parameters, METABOLISM including age at death of each individual and age of sexual maturity, that must be estimated either To date, the most thorough and complete from knowledge of living relatives or from approaches to analyzing the energetics of fossil detailed investigation of life-history as recorded assemblages have been outlined by Powell and by the shells of each species (seasonal growth Stanton (1985, 1996), Cummins et al. (1986), banding); and 2) completely size-censused fossil Staff et al. (1986), and Powell et al. (1992, 2001) assemblages. The latter limitation is particularly in a series of papers on the living mollusk problematic. The size-frequency distribution of communities and subfossil skeletal assemblages individuals is the most important piece of of Copano Bay, Texas, and adjacent shelf settings. information for estimating benthic energy fluxes This model, which estimates the total amount of (Powell and Stanton, 1985, 1996; Staff et al., energy assimilated by each individual in a fossil 1985; Cummins et al., 1986), and is also an assemblage over the course of its lifetime, has the attractive paleoecological parameter because the form: distribution of energy flow through size classes appears to be a more temporally persistent attribute of paleocommunity structure than (Eq. 3) relative abundance structure (Powell and Stanton, 1996). Unfortunately, although there are many Where A is the total amount of energy assimilated isolated case studies of within-assemblage size- by the individual over the course of its life, Pg is frequency distributions in the paleontological the proportion of lifetime net production allocated literature, they tend to focus on single species or to somatic tissue growth, Pr is the proportion of genera. Additional whole-assemblage studies are lifetime net production allocated to reproduction, feasible in exceptionally well-preserved units, and and R is the amount of energy respired over the would be a very useful contribution; meanwhile, a individual’s lifetime (Powell and Stanton, 1985, simpler approach may suffice to at least highlight 1996). Powell and Stanton (1985) used this broad trends. framework to estimate energy flow through four gastropod and one bivalve species preserved in Example I: Ordovician trilobites and the Eocene Stone City Formation, and showed brachiopods that relative ecological importance as measured Finnegan and Droser (2008) integrated genus- by energy flow differed substantially from level body size estimates with relative abundance ecological importance as measured by relative data from shallow to deep subtidal Laurentian abundance. fossil assemblages to examine Ordovician trends The framework established by Powell and in the biomass and metabolic demands of Stanton (1985) has several attractive properties. trilobites and brachiopods, the dominant Because the individuals in a death assemblage components of Sepkoski’s (1981) Cambrian and have, by definition, completed their lives, it Paleozoic Evolutionary Faunas (EF). Their attempts to account for lifetime energy analysis assumed that: 1) the maximum body size expenditures by integrating respiration, recorded for a genus in a given interval is a reproduction, and somatic growth costs from the reasonable proxy for the mean size of individuals age of larval settlement to the age of death. Large in that genus; 2) the total density of individuals on individuals in living assemblages have a the seafloor was constant or increasing through disproportionate influence on energy fluxes the Ordovician (a conservative assumption given because they account for a larger share of the biomass and bioturbation trends discussed instantaneous respiration and biomass production, above); and 3) fossil size-frequency distributions but this influence is magnified in the Powell and are, if not comparable to those of the original Stanton (1985) framework because large, dead living assemblages (a problematic assumption, as individuals represent the integration of energy previously discussed), subject to relatively expenditures over a longer timespan than smaller consistent preservational biases. dead individuals do. Unlike Powell and Stanton’s (1985) analytical The principal disadvantage of Powell and framework, Finnegan and Droser’s (2008) Stanton’s (1985) approach for delineating trends approach does not quantify integrated lifetime

37 THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19 348 SETH FINNEGAN AND350 MARY L. DROSER SETH FINNEGAN AND MARY L. DROSER signed a brachiopod relative richness of 0.01, Trilobite rel. abundance Trilobite respiration arelativeabundanceof0.001,abiomass of 0.01, an EU of 0.01, and a predicted popula- tion density of 0.0001. An alternative ap- proach is to combine collections by formation and calculate relative abundance, biomass, and EU from these pooled collections. This substantially reduces the number of data points but eliminates the need to account for missing values. Trends observed in pooled collections are very similar to those observed when all collections are treated independent- ly.

Results Consistent with previous studies, the aver- Brachiopod rel. abundance Brachiopod respiration age relative abundance of trilobites decreases by an order of magnitude between the Early Ordovician (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 Ordovician collections, but only 4% of individuals in the Late Ordovician, whereas brachiopods go from an average of 19% in the Early Ordovi- cian to 77% in the Late Ordovician. Relative genus richness trends are similar (Fig. 3A,B), though because of the low richness of all taxa in most samples (median genus richness ϭ 6), they vary over a comparatively limited range.

The average body sizes of both trilobites IGUREFIGURE 2. Temporal trends in the relative abundance of IGURE FIGUREF 12.—5.Ordovician Temporal trends trends in the in estimatedthe relative standing abundanceF 6. (left Temporal panels) trends and in in the the estimated estimatedenergy aggregate use metabolic and brachiopods increase substantially throughbiomasstrilobites of trilobites (A) and (A) brachiopods and brachiopods (B) in (B) shallow in shallow to deep(EU) of trilobites (A) and brachiopods (B) in shallow to energy requirementssubtidal mixed (right carbonate-clastic panels) of settings. trilobites The (top relative panels) and brachiopods (bottom panels) from shallow to deep the Ordovician (Churchill-Dickson 2001;to deep subtidal mixed carbonate-clastic settings. Bio- deep subtidal mixed carbonate-clastic settings. EU is subtidalmass Laurentianabundance is calculated of eachpaleocommunities.as mean group body is calculatedsize multiplied asWhereas a proportionby rel- thecalculated relative as mean abundance body size to of the trilobites¾ power multiplied declines considerably Stempien et al. 2005; Novack-Gottshallthroughout 2008a)ativeof abundance,the all individuals Ordovician, and in the the their resulting collection estimatedbiomass (including metabolicestimates trilobites, byenergy relative requirements abundance, and remain the resulting relatively EU estimates stable, a trend largely and this is expressed in our data set (Fig.are summedbrachiopods, for all and taxa other in each taxa). group. When If either a group group was wasare summed for all taxa in each group. If a group was driven entirely byentirely the missing missing presence from from a collect ofa collect ion, theion, it was exceptionally it was arbitrarily arbitrarily as- as-largeentirely asaphid missing from genus a collect Isotelusion, it was in arb itrarilymany as-Late Ordovician 4A,B). Consequently, trends in biomass depart paleocommunities.signedsigned a biomass a relative I1: of 489.0–476.50.01. abundance Boxes, whiskers, ofMa, 0.001. I2: circles, Relative476.5–472 and abun- signedMa, W1: an EU 472–470 of 0.01. Boxes, Ma, whiskers,W2: 470–460.5 circles, and Ma, time M1: 460.5–454.5 quite strikingly from relative richness andtimedances bins as for in Figureeach group 2. are logit-transformed. The endsbins as in Figure 2. abundance trends (Fig. 5A,B). MostMa, notably, M2: 454.5–451of the boxes Ma, mark C1: the 451–448.5 positions of theMa, first C2: and 448.5–444 third Ma. Modified from Finnegan and Droser (2005). quartiles, horizontal lines mark the median, whiskers the sharp decline in relative abundance of tri- extend 1.5 times the interquartile range (IQR) below the lobites is not mirrored by biomass estimates:energyof expenditures.brachiopodsfirst and above theincreases third Rather, quartile. substantially it Open focuses circles (Fig. are col-on2003; Herrmannand the abundance et al. 2004; of Saltzman the ith genus.and Respiration though total within-sample trilobite biomass6B).lections In estimating that fall less EU, than however, 1.5 · IQR the above tempera- or below theYoung 2005), and several of the Late Ordovi- estimatingmedian; the filled instantaneous circles are outliers. energy Time bins flux are as that fol- typically accounts for 30–80% of lifetime energy varies over five orders of magnitudewould in theture-sensitivity havelows: Ibexian been 1 ofϭ required489.0–476.5 metabolic Ma, toefficiency Ibexian maintain 2 ϭ(eq.476.5–472 3) thecian unitsexpenditures sampled in our in database marine have invertebrates been (Huebner sample set as a whole, the average biomass ofintroducesMa, Whiterockian a complicating 1 ϭ 472–470 factor. Ma, Whiterockian We have 2 ϭinterpreted as cool-water carbonates (Pope trilobites in Late Ordovician collectionsindividual isminimized470–460.5 metabolic the Ma, effects Mohawkian rates ofoflatitudinal 1allϭ 460.5–454.5individualsvariation Ma, Mohaw-in in theand Readand Edwards,1995; Holland 1981; and Barkai Patzkowsky and Griffiths, 1988; assemblagekian had 2 ϭ 454.5–451 they been Ma, Cincinnatian alive simultaneously. 1 ϭ 451–448.5 Ma, Morton and Chan, 1999) and although this within an order of magnitude of the Early Or-ourCincinnatian data set by 2 includingϭ 448.5–444 only Ma. collections from 1996). The earliest evidence of significant cool- dovician average. This istemperature-sensitive, based on a simple extension carbonate-dominated of Eq. 2 ining in Laurentiaapproach occurs does in not the late explicitly Mohawkian estimate biomass The sharp increase in average trilobitewhich body depositional per-genus settings metabolic within rate tropical estimates to sub- are(Pope andproduction Steffen 2003; rates, Saltzman there and is a Young moderately strong size in the upper Middle and Late Ordovicianweightedtropical nus by includes latitudes, their the relative but largest there is (or,known considerable if tri available,lobite ev- spe-2005) andpositive includes correlation a shift to more between positive mean annual is largely attributable to the widespreadabsolute) oc-idence ciesabundances: of (I. a rex lo),ng-term which attained cooling lengthstrend through- of up to 72␦18Oandrespiration␦13Cvalues(Shieldsetal. and production2003), ex-rates in animal currence of the exceptionally large asaphidoutcm much (Rudkin of the etLate al. Ordovician 2003). Though of Laurentia this speciespansionpopulations, of cherts and otherincluding upwelling-asso- marine invertebrates genus Isotelus.ThisexclusivelyLaurentiange-(Patzkowskydoes not appear et al. in 1997; our dataPope set, and the Steffen four spe-ciated(Humphreys, lithologies along 1979; the southernSchwinghamer margin, et al., 1986). Applying Eq. 4 to genera in Ordovician fossil (Eq. 4) assemblages reveals that, although the average relative abundance of trilobites declined where Bagg is the aggregate energy required for substantially over this interval as that of respiration, N is the total number of genera in the brachiopods increased, their average metabolic assemblage, B0i is a taxon specific normalization demand remained roughly constant (Fig. 12), a constant, and Mi and Ai are the mean body mass pattern driven primarily by occurrences of the widespread and exceptionally large asaphid genus

38 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS

Isotelus. In this case, focusing on biomass and Vermeij (1977, 1987, 2002, 2004), and others, the energetics rather than richness and abundance explosive Meso–Cenozoic diversification of the clarifies that the apparent displacement of Neogastropoda is particularly notable for its trilobites from an onshore setting by the radiating energetic implications. Whereas most Paleozoic Paleozoic fauna (Sepkoski and Sheehan, 1983; and early Mesozoic gastropods are thought to Sepkoski and Miller, 1985) was likely attributable have been detritivores and filter feeders, most to passive numerical dilution rather than modern marine gastropods are carnivores. The competitive interaction (Westrop et al., 1995). neogastropod diversification is a major component of the Phanerozoic increase in the Example II: Meso–Cenozoic gastropods proportion of predators in shelly fossil Finnegan et al. (2011) extended this approach assemblages (Bambach, 1985; Bambach et al., to evaluate the biomass and energetic 2002; Bambach and White, 2002), and implies requirements of gastropod assemblages from either a commensurate increase in primary before and after the Marine Mesozoic Revolution production and prey biomass, or competitive (Vermeij, 1977, 1987; Aberhan et al., 2006). To displacement of other nonskeletonized ameliorate the limitations imposed by lack of carnivorous groups. Assuming a typical trophic sufficient numbers of size-censused fossil transfer efficiency of ~10% and minimal assemblages, Finnegan et al. (2011) used size- gastropod-on-gastropod predation, Finnegan et al. frequency distributions of living gastropod (2011) estimated that the net primary production populations to parameterize a model relating the required to support respiration of an average maximum size of a species to its mean size. This gastropod individual rose as much as eightfold model was able to accurately predict the mean during the Mesozoic. Trends in primary individual sizes of nine fossil species from a size- productivity are difficult to estimate from fossil censused Middle Triassic assemblage. Using and geochemical records, but the diversification modeled mean-size estimates to generate species- trajectory of red group phytoplankton (Falkowski specific log-normal size distributions, and et al., 2004; Katz et al., 2004; van de assigning individual sizes by a random draw from Schootbrugge et al., 2005; van de Schootbrugge these distributions, Finnegan et al. (2011) broadly and Gollner, 2013) roughly coincides with the reproduced the modes and shapes of size- observed increase in gastropod size. censused gastropod assemblages. This is a promising approximation when individual size SUMMARY: CHALLENGES AND data are lacking, but requires further PROSPECTS parameterization and testing. Finnegan et al. (2011) modeled 432 fossil and 38 living or This review has covered only a handful of the subfossil tropical to subtropical gastropod many papers that pertain in one way or another to assemblages using this approach, and found that understanding the long-term patterns highlighted average individual metabolic rate increased from by Bambach (1993) two decades ago. Even with a a Lower Triassic low (Fraiser and Bottjer, 2004; narrow focus on the benthic marine record of Payne, 2005) to a Middle and Late Triassic skeletonized groups, the scope of the subject is so plateau, increased by ~150% between the Late broad that entire fields of study, such as Triassic and the Early Cretaceous (Fig. 13), then paleoceanography, micropaleontology,and remained relatively constant thereafter despite geochemistry that have much to say on this topic continued global diversification of gastropods. have been omitted. I have also tried to avoid This increase was driven primarily by a restating the qualitative arguments regarding substantial increase in both mean and maximum secular energetic trends already laid out by body size. The degree to which this reflects Bambach (1993) and others. These arguments are greater longevity versus faster growth rates is not as compelling today as they were twenty years known, but could be investigated by using stable ago, and the major advance in the interim has isotope sclerochronology to compare well- been the exponential growth of relevant data. preserved aragonitic individuals, such as those Quantification of energetic trends in the fossil from the Middle Triassic St. Cassian Formation record remains a very difficult problem that (Zardini, 1978; Nützel et al., 2010), with more involves aggregating disparate types of data that recent shells. are often fragmentary and poorly defined. Nearly As has been noted by Bambach (1993, 1996), all types of fossil data that are discussed here are

39 260 THE PALEONTOLOGICALSETH FINNEGAN SOCIETY ET AL. PAPERS, VOL. 19

IGURE B FIGUREF 6.13.— A,A) Boxplots Boxplots show showing the distribution the distribution of log10 mean of log individual10 mean individualmetabolic rate metabolic ( avg) for rate all assemblages(Bavg) estimates in each for Triassic,time interval. Early Bars, Jurassic, boxes, and and Late whiskers Cretaceous–Neogene as in Figure 5. Double-ended fossil gastropod arro w assemblages, marked ‘‘MMR’’ modern indicates shallow the interval subtidal over which the Mesozoic Marine Revolution occurred; break indicates a sampling gap of ,75 Myr between the Early tropical assemblages from St. Croix (Miller, 1988), and modern slope-abyssal assemblages from the northwest Jurassic and the Late Cretaceous. B, C, Bavg plotted against log10 of the total number of individualsth (B) andth species (C) Atlanticin each (McClain, assemblage. 2004). Black Horizontal circles 5 Early bars Triassic represent (n 5 median6); black values, diamonds boxes5 encloseMiddle Triassicthe 25 (throughn 5 16); black75 percentiles, squares 5 th th andLate whiskers Triassic indicate (n 5 58); the gray 2.5 circles and5 97.5Early percentiles. Jurassic (n 5 Double-ended9); gray diamonds arrow5 labeledLate Cretaceous MMR indicates (n 5 56); the white interval circles over5 whichEocene the ( n Mesozoic5 64); white Marine diamonds Revolution5 Neogene occurred; (n 5 break175), white indicates triangles a sampling5 Recent gap shallow of 75 subtidal Myr between (n 5 17); the white Early Jurassicinverted and triangles the Late5 RecentCretaceous. slope-abyssal B), C) B (avgn 5 plotted20). against: B) the total number of individuals; and C) species in each assemblage. Black circles = Early Triassic; black diamonds = Middle Triassic; black squares = Late Triassic; gray circles = Early Jurassic; gray diamonds = Late Cretaceous; white circles = Eocene; white diamonds = Neogene; whiteneogastropods triangles = Recent and St. ‘‘mesogastropods.’’ Croix; white inverted Both trianglesMiddle = Recent Triassic, slope-abyssal. and then Reproduced rises again with permissionbetween fromof theseFinnegan groups et al. (2011). have higher basal metabolic the Late Triassic and the Early Jurassic. Early rates on average than the less derived groups Jurassic samples already show a Bavg range characterizedthat dominate by extreme pre-MMR variability assemblages in time (Vladi- and similarlive-dead to the energetic Late Cretaceous–Neogene comparison encompassing range, a space.mirova This 2001),variability perhaps has many reflecting sources. theSome high of althoughbroader once range again of the environments small number would of Early be itrespiratory is attributable quotients to taphonomic associated information with diges-loss, Jurassicchallenging, samples but warrants would help caution. to answer As predict- critical which is a critical concern because paleoenergetic questions about the fidelity with which primary tion of animal tissue (Sterner and Elser 2002). ed by the hypothesis that the MMR represents estimates depend so heavily on interpretation of spatial and environmental energetic gradients are This transition is also reflected in proportions fossil abundance and body size distributions. apreserved unique and in the stepwise fossil record.increase It in is ecosystem likely that Taphonomicof carnivorous processes individuals and their (Fig. effect 5B; M-W on thep % energymuch of budgets, the abundance there and is little body-size change variation in Bavg in preservation0.001, K-S pof% diversity0.001; seeand additional abundance discussiongradients fromfossil the assemblages Late Cretaceous is not caused to the by taphonomic Neogene, havebelow), been asextensively has been studied previously (Toma discussedšových and by despitedistortion explosive but by genuine global gradients diversification that played ofas Kidwell,other workers 2009), (Vermeij but no specifically1977, 1987; Sohl energetic 1987; marineimportant gastropods, a role in controlling especially the neogastropods, distribution of comparisonBambach 1993, of living 2002; communities Bush et al. and 2007). their co- overhabitat, the nutrients, same interval and energy (Bambach in ancient 2002; oceans Sep- as occurringDriven death by assemblagesthese trends, has mean been per published capita koskithey do 2002). in modern Importantly, oceans. although For example, sample although size tometabolic date. Such rate a comparison (Bavg) estimates is feasible show with a sub-the variesthe Triassic–Recent over three orders increase of magnitudein the mean amongsize and Copanostantial Bay increase dataset compiled from the by Staff, Triassic Cummins, to the therespiration assemblages rate in ofour gastropods data set, the differences in shallow PowellNeogene, and colleagues, and the mean but thereB areof few pre- other and insubtropicalB distribution settings between is notable, pre- and there post- is datasets that include abundanceavg and individual considerableavg overlap in this metric between post-MMR intervals differs significantly MMR assemblages do not generally show a body size for both live and dead individuals—a Triassic and post-Jurassic assemblages, and the (Fig. 6A; M-W p % 0.001, K-S p % 0.001). strong dependence on sample size (Fig. 6B) or Mean Bavg rises from the Early Triassic to the species richness (Fig. 6C). 40 FINNEGAN: QUANTIFICATION OF ENERGY TRENDS IN ANCIENT ECOSYSTEMS differences between them are dwarfed by the Combined with the various field and analytical differences between modern shelf and abyssal approaches summarized here, these emerging faunas (Figs. 1, 13). Known environmental approaches have great potential to illuminate the gradients need to be controlled for in order to ways in which Earth systems processes have increase the likelihood of discerning temporal shaped the ecology and evolution of the marine signals above normal environmental noise. biota over time, and promise to make the next Despite the low signal/noise ratio, some features twenty years as exciting and productive as the last of this record have emerged as clear and robust: twenty years have been. increases in bioturbation intensity, bioclastic production, and mean body size associated with ACKNOWLEDGEMENTS the Ordovician Biodiversification are one example, as are the mirror-image trends I thank Andrew Bush, Jonathan Payne, and Sara associated with the Permo–Triassic extinction and Pruss for inviting me to participate in the short recovery interval. Other features of the fossil course. This manuscript benefitted from helpful record, such as the diffuse and protracted but reviews by Matthew Clapham and Shanan Peters cumulatively large changes in marine ecosystems and editorial feedback from Jonathan Payne. I associated with the Marine Mesozoic Revolution, also thank Thomas Brey for making the data in are still comparatively enigmatic and poorly his compilation of metabolic rate measurements defined (Aberhan et al., 2006). available to me. Numerous drivers that have been suggested as explanations for some of these trends have not REFERENCES been discussed, and include, but are not limited to, climate change (via its numerous potential ABERHAN, M., W. KIESSLING, A N D F. T. FÜRSICH. 2006. effects on primary productivity, the efficiency of Testing the role of biological interactions in the export of net primary production to benthic evolution of mid-Mesozoic marine benthic ecosystems, body size, and respiration efficiency), ecosystems. 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The statistical analysis of some of these hypotheses (e.g., the Jurassic compositional data (with discussion). Journal of increase in gastropod body size and biomass the Royal Statistical Society Series B (Statistical Methodology), 44:139–177. noted by Finnegan et al. (2011) and Kosnik et al. ALBERT, J. A., AND D. M. JOHNSON. 2012. Diversity (2011) is too early to have been driven by and evolution of body size in fishes. Evolutionary increased nutrient flux from Cretaceous expansion Biology, 39:324–340. of terrestrial angiosperms (Bambach, 1993, ALGEO, T. J., AND S. E. SCHECKLER. 1998. Terrestrial- 1999)), testing them more rigorously will require marine teleconnections in the Devonian: links more and better resolved paleobiological and between the evolution of land plants, weathering environmental proxy data, and more sophisticated processes, and marine anoxic events. models than are currently available. 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