Determinants of species abundance in the Quaternary vertebrate fossil ...

Paleobiology, 37(3), 2011, pp. 537–546

Determinants of species abundance in the Quaternary vertebrate fossil record Samuel T. Turvey and Tim M. Blackburn

Abstract.—Species abundance data are of vital importance in paleontology, but fossil accumulations invariably represent a biased subset of original source communities. Efforts to quantify taphonomic biases are typically prevented by a lack of independent data on the ecological composition of prehistoric faunas. However, analysis of the continental Holocene record can provide a rare opportunity for independent calibration of fossil abundance patterns. We analyzed a comprehensive data set available for the Holocene avifauna of Sweden to investigate the relationship between species abundance in the recent fossil and zooarchaeological records and in prehistoric source communities, and to characterize the importance of different ecological factors in determining terrestrial vertebrate fossil abundances. The number of assemblages in which species occurred was compared with modern-day species abundance, annual residence, body mass, and ecological realm. Modern-day abundance is only one of several significant predictors of fossil abundance; the strongest predictor is body mass, and Holocene species abundance can be interpreted as a measure of species abundance in source communities for a given size class only. Our study represents one of the only direct attempts to quantify species abundance biases between fossil faunas and source communities, and has general applicability for a wide range of terrestrial vertebrate faunas. Samuel T. Turvey* and Tim M. Blackburn. Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, United Kingdom. E-mail: [email protected]. *Corresponding author Accepted: 22 November 2010

Introduction Species abundance is one of the most fundamental concerns of ecology. Efforts to understand regional and global patterns of commonness and rarity have been central to the development of ecological disciplines as diverse as biogeography, population biology, macroecology, and conservation biology (e.g., MacArthur 1957, 1960; Preston 1962; Sugihara 1980; Soule´ 1986; Kunin and Gaston 1997). Species abundance data from the fossil record are also of vital importance in paleontology, and have formed the basis for analyses of macroevolution, faunal turnover and mass extinction (Wignall and Benton 1999; Jernvall and Fortelius 2002; Lockwood 2003; Vermeij and Herbert 2004); reconstructing the ecology of extinct species and communities (Bakker 1973; Carbone et al. 2009); and investigating the ecological impacts of prehistoric humans (Grayson 2001; Duncan et al. 2002; Broughton 2004; Newsome et al. 2007). However, the fossil record is notoriously incomplete (Darwin 1859; Kidwell and Flessa 1995; Kemp 1999; Briggs and Crowther 2001). ’ 2011 The Paleontological Society. All rights reserved.

Fossil accumulations invariably represent only a subset of the original fauna present in a given region at the time of deposition, and it is a subset that is likely to be biased. Taphonomic incompleteness leads to differential species sampling at a range of ecological scales, as a result of variable modification and preservation between death, burial, and subsequent long-term fossilization in different depositional environments in response to a wide range of varying physical, chemical, and/or biological processes (Andrews 1990; Behrensmeyer 1991; Martin 1999; Behrensmeyer et al. 2000). Absolute species abundances are almost impossible to ascertain from the fossil record, and even patterns of relative abundance must be treated with caution. This presents a fundamental constraint to generating data on prehistoric biodiversity and ecosystem properties that can be compared meaningfully with presentday systems. Attempting to understand the factors that determine species abundance in the fossil record has represented a long-standing challenge to paleontology. The biological and 0094-8373/11/3703–0012/$1.00

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ecological characteristics of species that might be expected to be either underrepresented or overrepresented in fossil deposits have in many cases been adequately characterized (Andrews 1990; Behrensmeyer 1991; Simms 1994; Behrensmeyer et al. 2005); analysis of differential patterns of faunal preservation in different deposits derived from the same source community has led to more meaningful reconstruction of specific ecosystems (e.g., Munõz-Durań and Van Valkenburgh 2006); and modeling the formation of fossil assemblages in order to diagnose their fidelity to source communities has also been attempted (Damuth 1982). However, efforts to quantify preservational biases in species abundance between fossil faunas and source communities have been almost completely prevented by a lack of any independent data on the ecological composition of prehistoric faunas other than that provided by the fossil record itself. Such studies as do exist have so far been limited to proxy investigations of abundances of dead remains, notably mollusc shells, in modern benthic and terrestrial environments (Kidwell and Flessa 1995; Kidwell 2001; Western and Behrensmeyer 2009). There is still little known about absolute abundance patterns in prehistoric vertebrate faunas, even in the late Quaternary fossil record, which can in many cases provide a remarkable level of information about the biology and ecology of extinct species from novel sources of data only rarely available in older deposits (Turvey and Cooper 2009). Developing a better understanding of true vertebrate abundances in late Quaternary ecosystems is of particular importance because these faunas have been severely affected by continent-wide extinction events from the late Pleistocene onward, while the ecological dynamics and drivers of these extinctions, and in particular the extent of anthropological involvement, continue to be the subject of considerable dispute (e.g., MacPhee 1999; Grayson 2001; Barnosky et al. 2004; Turvey 2009). Unfortunately, most prehistoric late Quaternary vertebrate faunas exhibit substantial qualitative differences from faunas present in the same geographical regions today, confounding quantitative comparison between

past and present patterns of species abundance. Late Pleistocene faunas occurred in glacial-era environments, with some biomes and faunal communities having no modernday analogs (Stafford et al. 1999; Graham 2005). Holocene faunas occurred under interglacial climatic conditions similar to those of the present day, but most vertebrate faunas of particular interest to paleontologists (notably island faunas) have been heavily modified by prehistoric or historical-era human-driven extinctions, so that modern-day species diversity and abundances do not reflect prehuman patterns in these regions (MacPhee and Flemming 1999; Turvey 2009). Conversely, although continental Holocene vertebrate faunas have also sustained species losses and population reductions, particularly as human pressures have escalated during recent history (Morrison et al. 2007), in many cases faunas occurring since the end of the Late Glacial are expected to be closely comparable to those present in the same regions today, because climatic and environmental variability has been relatively minor during this interval in comparison with earlier Quaternary conditions (Roberts 1998). For continental regions where fossil faunas have been adequately documented and accurate abundance data are also available for modern-day faunas, analysis of the Holocene record can therefore provide a rare opportunity for independent calibration of abundance patterns represented in the fossil record. Both Holocene and modern-day vertebrate faunas have been well studied in much of the Western Palearctic. Within this region, a particularly comprehensive review is available for the Holocene avifauna of Sweden (Ericson and Tyrberg 2004), representing a highly detailed data set for which avian species diversity is reported for 531 Holocene fossil and zooarchaeological assemblages (either separate sites or distinct stratigraphic levels within complex sites) spanning the Preboreal, Boreal, Atlantic, Subboreal, and Subatlantic chronozones from across the country (Fig. 1). There have been some documented changes to the Swedish avifauna across this interval, notably the regional or global extinction of the great auk (Pinguinus

DETERMINANTS OF FOSSIL SPECIES ABUNDANCE

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Tyrberg 2004). It therefore constitutes an ideal study system for investigating the relationship between species abundance in the recent fossil record and in prehistoric source communities, and for characterizing the importance of different ecological and taphonomic factors in determining terrestrial vertebrate fossil abundances. Material and Methods

FIGURE 1. Locations of 531 Holocene sites in Sweden containing fossil or zooarchaeological bird remains.

impennis), Dalmatian pelican (Pelecanus crispus) and gadfly petrel (Pterodroma cf. feae), the human-assisted introduction of five domesticated bird taxa, and avifaunal responses to shifts in forest cover and structure driven by climatic fluctuations and agricultural intensification. However, this avifauna has remained largely stable for ,9000 years (Ericson and

A data set of Swedish bird species abundances in the Holocene record was compiled from avian species lists available for Holocene assemblages reviewed by Ericson and Tyrberg (2004), which provide information on species presence/absence in each assemblage (see supplemental information online at http:// dx.doi.org/10.1666/09075.s1). All provisional or tentative species identifications of avian osteological material were interpreted as being definite identifications for the purposes of analysis. The number of fossil assemblages in which each bird species occurred was used as the metric of Holocene abundance. Although this is technically a measure of species distribution rather than species abundance, these two variables are typically strongly positively correlated, especially at the national scale and when distribution is measured as number of occupied sites (Blackburn et al. 2006). Although many Swedish Holocene sites consist of zooarchaeological assemblages, these are mainly kitchen middens or similar deposits in prehistoric settlements. Thus, they can be interpreted as a form of predator accumulation equivalent in taphonomic bias to many ‘‘natural’’ Quaternary deposits (Lyman 1994; Simms 1994). However, 84 sites containing avifaunal remains represent specific human burial sites, often aristocratic graves, and display more extreme faunal biases through the deliberate burial of raptors involved in falconry/hawking or as lures for hunting corvids (Ericson and Tyrberg 2004). Of the bird species represented relatively abundantly in Swedish Holocene assemblages (found in at least ten assemblages), over 70% of all eagle owl (Bubo bubo) records and ,50% of all goshawk (Accipiter gentilis) and peregrine falcon (Falco peregrinus) records are from such ‘‘falconry graves,’’ and several

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other species are also overrepresented in comparison to non-burial assemblages. Although the relationship between avifaunal occurrence in log(1 + total Holocene assemblages) and log(1 + non-burial assemblages) is very strong (r2 5 0.99, n 5 265, p % 0.001, linear regression estimate 5 0.963 6 0.006), and there is a significant positive relationship between occurrence in log(1 + non-burial assemblages) and log(1 + burial assemblages) (r2 5 0.37, n 5 265, p % 0.001, linear regression estimate 5 1.368 6 0.109), specific grave sites were excluded from analysis to reduce the amount of ‘‘non-natural’’ bias in the Holocene data. A number of problematic taxa had to be excluded from the Holocene data set. Zooarchaeological records of domestic fowl (Gallus gallus), turkey (Meleagris gallopavo), and peacock (Pavo muticus) were excluded because they are not representatives of the native Swedish avifauna. Two other bird species, greylag goose (Anser anser) and mallard (Anas platyrhynchos), are native to Sweden but were also present as domestic forms during the Holocene, and in both cases wild and domestic forms are difficult or impossible to separate osteologically (Barnes and Young 2000; Ericson and Tyrberg 2004). The mallard was retained in the data set because the earliest north European records of domestic ducks date only from the medieval period (Zeuner 1963) and all Swedish assemblage records where this is not the only bird present also include non-domesticated species, suggesting that most of the Swedish Holocene mallard records may also represent wild individuals. Conversely, domestic geese were introduced to Sweden much earlier, in the Bronze Age or Iron Age, and are frequently found at Swedish sites only in association with Gallus gallus in a clearly domestic context (Ericson and Tyrberg 2004). All data for Anser anser were therefore excluded. Two human commensals, house sparrow (Passer domesticus) and feral pigeon (Columba livia), have probably never been natural breeding birds in Sweden (Ericson and Tyrberg 2004), but were retained for analysis because past Holocene population data can be compared meaningfully with

modern-day data. Two other originally nonEuropean species that have become established as wild populations in Sweden only in the recent historical era, the common pheasant (Phasianus colchicus) and collared dove (Streptopelia decaocto), are absent from the Swedish Holocene record. These were also excluded from analysis, together with the three Holocene bird species that are now extinct in Sweden (great auk, Dalmatian pelican, and gadfly petrel). The number of assemblages in which each species occurred was compared with four predictor variables: modern-day bird species abundance, annual residence, body mass, and ecological realm. Modern-day abundance was compiled by combining data on mean breeding population size estimates (breeding pairs 3 2) and mean winter population size estimates for Swedish birds given by BirdLife International (2004). For 240 of the 256 species recorded by BirdLife (2004) as currently being present in Sweden, population size estimates were provided for only one of these two categories, and we used this figure as the species’ modern abundance. For the remaining 16 species, these two modern-day abundance estimates differ markedly and can be interpreted as independent estimates of different populations of breeding or wintering birds present in the study region at different times of year, and so the breeding and wintering population sizes were summed. Abundance was log(n + 1) transformed for analysis. Residence is a measure of whether bird species are present in Sweden all year, either as resident populations or as distinct breeding and wintering populations, or whether they are only present as seasonal migrant populations for part of the year; data were compiled from Lokki and Palmgren (1989). Body mass data were taken from Dunning (2007). Mean female mass was used preferentially, but if this was unavailable for a species then mean mass derived from samples including both sexes, or where sex was unclassified, was used. Body mass was logarithmically transformed for analysis. For the final predictor variable, realm, species were classified as to whether or not they spend a substantial part


of the year at sea (either foraging or wintering). We might expect such species (largely in the families Gaviidae, Procellariidae, Anatidae, Laridae, and Alcidae) to occur in fewer Holocene assemblages than species that spend the great majority of their time on land. Determinants of the number of assemblages in which each species occurred were assessed in three ways. First, using a general linear model (GLM), we analyzed the individual effect of each of the four predictor variables on the number of natural fossil assemblages in which a species is found. Because the response variable is a count, simple linear regression methods are not appropriate; they can lead to predictions of negative counts, because the variance of the response is likely to increase with its mean, and because model errors will not be normally distributed. Thus, we analyzed the number of natural fossil assemblages as a count variable using quasipoisson errors and a log-link. We used quasipoisson rather than Poisson errors to cope with overdispersion (extra unexplained variation) in the response variable. Second, because it is unlikely that each of the four predictor variables is independent of the other (e.g., small-bodied bird species tend to be more abundant than large-bodied species, on average [Gaston and Blackburn 2000]), we produced a multivariate general linear model (GLM) of number of natural fossil assemblages occupied in terms of the predictors. Nonsignificant variables were deleted to produce a minimum adequate model of number of assemblages in which a species occurred in terms only of variables that explain significant independent variation in the response. Third, we produced a multivariate general linear mixed model (GLMM) of number of assemblages in terms of the four predictor variables described above, with the response analyzed as a count variable using quasipoisson errors and a log-link, and the taxonomic levels order, family, and genus included as nested random effects. Variables were again deleted, this time to produce the model with the lowest Akaike’s information criterion (AIC). We used the GLMM approach to

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account for the possibility that closely related species may be found in similar numbers of assemblages because of characteristics they share through common ancestry (e.g., body mass), and hence do not comprise independent pieces of information as is required by conventional GLM analysis. Classification to genus, family, and order followed Sibley and Monroe (1990). In fact, variance components analysis shows that most variance in the number of assemblages in which a species occurs is found at low taxonomic levels (45.0% across species within genera, 20.1% across genera within families, 10.2% across families within orders, and 24.7% across orders). Further, none of the random effects of taxonomy were significant. Although this suggests that a GLM approach is likely to be sufficient, we report the results of the GLMM analysis for the sake of completeness. Model criticism identified the mute swan (Cygnus olor) as a consistent large outlier, and so this species is excluded from the results reported below. The sample size for all analyses is 265 species. Analyses were performed in R, version 2.7.1 (R Development Core Team 2006). The GLMM was implemented using the lmer command in the lme4 package. Results The number of assemblages in which each bird species occurred was significantly positively related to modern day abundance (regression estimate 6 standard error 5 0.092 6 0.033, p , 0.01) and body mass (0.617 6 0.052, p % 0.001), and was higher for resident species (1.591 6 0.252, p % 0.001) and for species spending substantial parts of the year in the marine realm (20.910 6 0.289, p , 0.01) (Fig. 2). The full GLM revealed significant effects on number of assemblages of all predictor variables except realm; the reduced model with realm excluded is shown in Table 1. As an estimate of model fit (Zheng and Agresti 2000), the squared correlation between the predicted and actual values of the number of assemblages in which each bird species occurred is 0.39. A GLMM with modern-day abundance, body mass, residence, and realm included as

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FIGURE 2. The relationship between the number of natural fossil localities in which a species occurs, and each of the four modern biological or ecological predictors of this number. Data for realm and residence are log-transformed for clarity. The regression lines for modern abundance and body mass are from the respective univariate GLM models with quasipoisson errors reported in ‘‘Results.’’

fixed effects, and the taxonomic levels order, family, and genus included as random effects, also revealed significant effects on number of assemblages of all predictor variables except realm. Removing realm produced the model with the lowest AIC (Table 2). Thus, all TABLE 1. Minimum adequate GLM of number of assemblages in which a species is found. The number of assemblages is analyzed as a count variable using quasipoisson errors and a log-link.

Intercept Log (1 + abundance) Log body mass Residence

Estimate

SE

t

25.932 0.261 0.821 0.494

0.455 0.024 0.045 0.152

213.04*** 10.78*** 18.26*** 3.26**

* p , 0.05, ** p , 0.01, *** p , 0.001.

analyses concur that resident bird species with larger body masses and higher modernday Swedish abundances occur in more Swedish Holocene assemblages. Discussion Species abundance is a phylogenetically labile trait that can differ markedly between even the most closely related species: variance components analysis on the modern Swedish abundance data shows that 72.5% of the variance in abundance clusters at the species level, versus 24.5% at the order level and above (the other few percent falls at the genus and family levels). The abundance of a given species can also show rapid temporal


TABLE 2. Minimum adequate GLMM of number of assemblages in which a species is found. The response is analyzed as a count variable using quasipoisson errors and a log-link, and the taxonomic levels order, family, and genus are included as nested random effects. Fixed effects

Estimate

SE

t

Intercept Log (1 + abundance) Log body mass Residence

25.576 0.256 0.762 0.226

0.321 0.014 0.043 0.094

217.42*** 18.64*** 17.79*** 2.41*

Variance

SD

0.120 0.127 0.217 0.528

0.346 0.357 0.465 0.727

Random effects Order Family Genus Residual

* p , 0.05, ** p , 0.01, *** p , 0.001.

changes, as demonstrated by the colonization of most of Europe by the collared dove over the course of about a century (Hengeveld 1989). However, the relative abundances of most species in many assemblages stay largely unchanged over long periods of time (Miller 1996; DiMichele et al. 2004), and Ericson and Tyrberg (2004) considered this to be true of the Swedish avifauna for most of the Holocene. If so, then modern-day species abundance constitutes a meaningful proxy for past abundance in autochthonous bird source communities at the time of Holocene fossil deposition. Modern-day species abundance is significantly correlated with bird species abundance in Holocene fossil and zooarchaeological assemblages. Modern-day abundance is, however, only one of a series of ecological predictors of bird species abundance in the recent fossil record. On its own, it is a relatively weak predictor. In univariate analyses, all of the other variables tested against abundance in Holocene assemblages were also significant, and both body mass and, somewhat less so, residence had greater predictive value than modern-day abundance. The standard Pearson correlation coefficient for the relationship between occurrence in the fossil record and modern-day abundance is 0.15, versus 0.50 for body mass (although these results should not be overinterpreted as this is an inappropriate statistical test given the structure of the data). Body mass is also a strong predictor in multivariate models of the number of Holo-

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cene assemblages in which a bird species is found (Tables 1, 2). Its importance is ably demonstrated by the fact that only five Holocene fossil finds are known for all of Sweden’s six most abundant bird species combined (willow warbler Phylloscopus trochilus, chaffinch Fringilla coelebs, tree pipit Anthus trivialis, robin Erithacus rubecula, goldcrest Regulus regulus, and great tit Parus major), which together comprise over 50% of all bird individuals in the modern-day Swedish avifauna (BirdLife International 2004), but each of which weighs less than 30g. For the country’s avifauna as a whole, only 35% of passerine species compared to 59% of typically larger-bodied non-passerine species have been definitely or questionably reported from Holocene assemblages (Ericson and Tyrberg 2004). If mass is controlled for, however, then the influence of modern-day abundance is greatly increased, while the effects of residence and realm are decreased. Species abundance in the recent fossil record can therefore be interpreted as a measure of species abundance at the time of fossil deposition, but for a given avian size class only. Modern-day abundance, residence, and realm can all be viewed as measures of the availability of individuals to pass through the process of fossil preservation. In this regard, the unexpected effect shown by realm, where seagoing birds are more abundantly represented in the Holocene record than terrestrial birds, may reflect the relative abundance of coastal sites in Sweden (Fig. 1) and the extensive regional human exploitation of marine bird resources evidenced in coastal midden deposits in other parts of the world (see Broughton 2004). However, the significant effect of realm is probably more likely to have arisen through its correlation with body mass, because sea-going birds are relatively large bodied (ANOVA, F1263 5 27.02, p % 0.001; see also Gaston and Blackburn 2005), and this predictor variable becomes nonsignificant when body size is also included in multivariate analyses. The strong effect of body mass in explaining avian species abundance in the Holocene record is likely to be due to several different processes operating at all stages of the taphonomic history of a faunal assemblage.

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First, even though small-bodied birds such as starlings (Sturnus vulgaris) may have been preferentially preserved as cage birds in some zooarchaeological assemblages (Ericson and Tyrberg 2004), preferential hunting of largerbodied species by humans and other predators will typically restrict the number of smaller species that are capable of being buried in middens and many other predator accumulation sites (Duncan et al. 2002; Broughton 2004). The commonest bird species from Swedish sites are grouse (capercaillie Tetrao urogallus, black grouse Tetrao tetrix), waterfowl (mallard, eider Somateria mollissima, goldeneye Bucephala clangula, whooper swan Cygnus cygnus, common merganser Mergus merganser, velvet scoter Melanitta fusca, red-breasted merganser Mergus serrator), and great cormorant (Phalacrocorax carbo), all species that would have constituted favored prey species for human hunters. Raptor deposits are a rich source of microvertebrate remains in the late Quaternary record (Andrews 1990; Simms 1994), but relatively few ancient raptor sites containing bird remains have been identified from the region (Ericson and Tyrberg 2004). Second, robust skeletal elements from larger-bodied species are more likely to survive early structural or bone-density-mediated destructive processes. The minute, fragile bones of small-bodied taxa such as passerines have a diminished preservation potential in many depositional environments (Duncan et al. 2002; Behrensmeyer et al. 2000, 2005). Third, although species identification from osteological information in the absence of soft-tissue characters is a widespread problem for all avian taxa, and some small-bodied passerines (e.g., Coccothraustes) are osteologically distinctive, even in the well-studied Western Palearctic late Quaternary avian record it remains extremely difficult if not impossible to identify many passerine genera (e.g., Anthus, Emberiza, Motacilla, Phylloscopus, Sylvia) to species level on the basis of skeletal remains (Ericson and Tyrberg 2004). Finally, even if diagnostic elements of small-bodied species are sufficiently preserved in the fossil record, a human-sampled

collection of fossil material from a given site is still likely to underrepresent these taxa. Early collectors were often most interested in obtaining the remains of large charismatic species, and many late Quaternary sites have historically been sampled in a non-systematic manner without fine-meshed screens to collect tiny skeletal elements. Our study represents one of the only direct attempts to quantify preservational biases in species abundance between fossil faunas and source communities, and has characterized the relative significance of different ecological and taphonomic factors in determining the composition of Holocene avian fossil assemblages. Our findings on the fidelity of species abundances from the fossil record based on continental bird data are likely to have general applicability for understanding vertebrate faunas from Quaternary and older geological deposits in both continental and insular systems. The Swedish Holocene record consists of both natural and zooarchaeological assemblages, and so is taphonomically comparable to Holocene faunal data available for other regions of particular interest to Quaternary paleontologists (cf. Worthy and Holdaway 2002; Newsom and Wing 2004; Steadman 2006). Although seasonal variation in abundance due to migration represents an ecological characteristic of many continental bird species that can confound interpretation of fossil abundance data (Cooper 2005) and is less significant in other terrestrial vertebrate communities (e.g., endemic avian island communities), we have controlled for this effect in our analysis by combining summering and wintering bird population data and by including a separate predictor variable for residence. Species identification of smallbodied mammal fossils may be more feasible on the basis of tooth characteristics absent in birds if diagnostic craniodental elements are available, but other general biases against the burial, preservation, and post-burial collection of these taxa are still expected to apply. Similarly, although specific types of deposits such as raptor accumulations may be underrepresented in the Swedish record in comparison to other geographical regions (e.g., islands with significant karst limestone cave


systems), the strength of the statistical effects of body mass and other predictor variables demonstrated in this study confirms that similar taphonomic biases in faunal preservation may also be expected under such alternative conditions. We emphasize that interpreting species abundance data from the fossil record is not straightforward and should not be conducted ‘‘at face value,’’ and in particular that species body mass has a confounding effect on the fidelity of fossil assemblages to prehistoric source communities. This has profound implications for all studies that use fossil abundance data to draw conclusions about patterns of ecology, community structure, evolution, and extinction over time. Acknowledgments We thank J. Cooper, T. Tyrberg, and an anonymous referee for discussion and suggestions. Support for this project was provided by a NERC Postdoctoral Fellowship. Literature Cited Andrews, P. 1990. Owls, caves and fossils. Natural History Museum Publications, London. Bakker, R. T. 1973. Anatomical and ecological evidence of endothermy in dinosaurs. Nature 238:81–85. Barnes, I., and J. P. W. Young. 2000. DNA-based identification of goose species from two archaeological sites in Lincolnshire. Journal of Archaeological Science 27:91–100. Barnosky, A. D., P. L. Koch, R. S. Feranec, S. L. Wing, and A. B. Shabel. 2004. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306:70–75. Behrensmeyer, A. K. 1991. Terrestrial vertebrate accumulations. Pp. 291–335 in P. A. Allison and D. E. G. Briggs, eds. Taphonomy: releasing the data locked in the fossil record. Plenum, New York. Behrensmeyer, A. K., S. M. Kidwell, and R. A. Gastaldo. 2000. In D. H. Erwin and S. L. Wing, eds. Deep time: Paleobiology’s perspective. Paleobiology 26(Suppl. to No. 4):103–147. Behrensmeyer, A. K., F. T. Fu¨rsich, R. A. Gastaldo, S. M. Kidwell, M. A. Kosnik, M. Kowalewski, R. E. Plotnick, R. R. Rogers, and J. Alroy. 2005. Are the most durable shelly taxa also the most common in the marine fossil record? Paleobiology 31:607–623. BirdLife International. 2004. Birds in Europe: population estimates, trends and conservation status. BirdLife Conservation Series No. 12. BirdLife International, Cambridge, U.K. Blackburn, T. M., P. Cassey, and K. J. Gaston. 2006. Variations on a theme: sources of heterogeneity in the form of the interspecific relationship between abundance and distribution. Journal of Animal Ecology 75:1426–1439. Briggs, D. E. G., and P. R. Crowther, eds. 2001. Palaeobiology II. Blackwell Science, Oxford. Broughton, J. M. 2004. Prehistoric human impacts on California birds: evidence from the Emeryville Shellmound midden. Ornithological Monographs 56:1–90.

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Carbone, C., T. Maddox, P. J. Funston, M. G. L. Mills, G. F. Grether, and B. Van Valkenburgh. 2009. Parallels between playbacks and Pleistocene tar seeps suggest sociality in an extinct sabretooth cat, Smilodon. Biology Letters 5:81–85. Cooper, J. 2005. Pigeons and pelagics: interpreting the Late Pleistocene avifaunas of the continental ‘island’ of Gibraltar. Monografies de la Societat d’Histo`ria Natural de les Balears 12:101–112. Damuth, J. 1982. Analysis of the preservation of community structure in assemblages of fossil mammals. Paleobiology 8:434–446. Darwin, C. 1859. On the origin of species by means of natural selection, or the preservation of favored races in the struggle for life. John Murray, London. DiMichele, W. A., A. Behrensmeyer, T. D. Olszewski, C. C. Labandeira, J. M. Pandolfi, S. L. Wing, and R. Bobe. 2004. Longterm stasis in ecological assemblages: evidence from the fossil record. Annual Review of Ecology, Evolution, and Systematics 35:285–322. Duncan, R. P., T. M. Blackburn, and T. H. Worthy. 2002. Prehistoric bird extinctions and human hunting. Proceedings of the Royal Society of London B 269:517–521. Dunning, J. B. 2007. CRC handbook of avian body masses, 2d ed. CRC Press, Boca Raton, Fla. Ericson, P. G. P., and T. Tyrberg. 2004. The early history of the Swedish avifauna: a review of the subfossil record and early written sources. Kungliga Vitterhets Historie och Antikvitets Akademiens Handlingar, Antikvariska Serien 45:1–349. Gaston, K. J., and T. M. Blackburn. 1995. The frequency distribution of bird body weights: aquatic and terrestrial species. Ibis 137:237–240. ———. 2000. Pattern and process in macroecology. Blackwell Science, Oxford. Graham, R. W. 2005. Quaternary mammal communities: relevance of the individualistic response and non-analog faunas. Paleontological Society Papers 11:141–158. Grayson, D. K. 2001. The archaeological record of human impacts on animal populations. Journal of World Prehistory 15:1–68. Hengeveld, R. 1989. Dynamics of biological invasions. Chapman and Hall, London. Jernvall, J., and M. Fortelius. 2002. Common mammals drive the evolutionary increase of hypsodonty in the Neogene. Nature 417:538–540. Kemp, T. S. 1999. Fossils and evolution. Oxford University Press, Oxford. Kidwell, S. M. 2001. Preservation of species abundance in marine death assemblages. Science 294:1091–1094. Kidwell, S. M., and K. W. Flessa. 1995. The quality of the fossil record: populations, species, and communities. Annual Review of Ecology and Systematics 26:269–299. Kunin, W. E., and K. J. Gaston, eds. 1997. The biology of rarity: causes and consequences of rare-common differences. Chapman and Hall, London. Lockwood, R. 2003. Abundance not linked to survival across the end-Cretaceous mass extinction: patterns in North American bivalves. Proceedings of the National Academy of Sciences USA 100:2478–2482. Lokki, J., and J. Palmgren. 1989. Suomen ja pohjolan linnut. Werner So¨derstro¨m Osakeyhtio¨, Helsinki. Lyman, R. L. 1994. Vertebrate taphonomy (Cambridge Manuals in Archaeology). Cambridge University Press, Cambridge. MacArthur, R. H. 1957. On the relative abundance of species. Proceedings of the National Academy of Sciences USA 43:293. ———. 1960. On the relative abundance of species. American Naturalist 94:25–36. MacPhee, R. D. E., ed. 1999. Extinctions in near time: causes, contexts, and consequences. Kluwer Academic/Plenum, New York.

546


MacPhee, R. D. E., and C. Flemming. 1999. Requiem æternam: the last five hundred years of mammalian species extinctions. Pp. 333–371 in R. D. E. MacPhee, ed. Extinctions in near time: causes, contexts, and consequences. Kluwer Academic/Plenum, New York. Martin, R. E. 1999. Taphonomy: a process approach. Cambridge University Press, Cambridge. Miller, W., III. 1996. Ecology of coordinated stasis. Palaeogeography, Palaeoclimatology, Palaeoecology 127:177–190. Morrison, J. C., W. Sechrest, E. Dinerstein, D. S. Wilcove, and J. F. Lamoreux. 2007. Persistence of large mammal faunas as indicators of global human impacts. Journal of Mammalogy 88:1363–1380. Munõz-Durań, J., and B. Van Valkenburgh. 2006. The Rancholabrean record of Carnivora: taphonomic effect of body size, habitat breadth, and the preservation potential of caves. Palaios 21:424–430. Newsom, L. A., and E. S. Wing. 2004. On land and sea: Native American uses of biological resources in the West Indies. University of Alabama Press, Tuscaloosa and London. Newsome, S. D., M. A. Etnier, D. Gifford-Gonzalez, D. L. Phillips, M. van Tuinen, E. A. Hadly, D. P. Costa, D. J. Kennett, T. P. Guilderson, and P. L. Koch. 2007. The shifting baseline of northern fur seal (Callorhinus ursinus) ecology in the northeast Pacific Ocean. Proceedings of the National Academy of Sciences USA 104:9709–9714. Preston, F. W. 1962. The canonical distribution of commonness and rarity. Ecology 43:185–215, 410–432. R Development Core Team. 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Roberts, N. 1998. The Holocene: an environmental history. WileyBlackwell, Oxford. Sibley, C. G., and B. L. Monroe. 1990. Distribution and taxonomy of birds of the world. Yale University Press, New Haven, Conn.

Simms, M. J. 1994. Emplacement and preservation of vertebrates in caves and fissures. Zoological Journal of the Linnean Society 112:261–283. Soule´, M. E., ed. 1986. Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, Mass. Stafford, T. M., Jr., H. A. Semken Jr., R. W. Graham, W. F. Klipel, A. Markova, N. Smirnov, and J. Southon. 1999. First accelerator mass spectrometry 14C dates documenting contemporaneity of nonanalog species in late Pleistocene mammal communities. Geology 27:903–906. Steadman, D. W. 2006. Extinction and biogeography of tropical Pacific birds. University of Chicago Press, Chicago. Sugihara, G. 1980. Minimal community structure: an explanation of species abundance patterns. American Naturalist 116:770–787. Turvey, S. T. 2009. In the shadow of the megafauna: prehistoric mammal and bird extinctions across the Holocene. Pp. 17–39 in S. T. Turvey, ed. Holocene extinctions. Oxford University Press, Oxford. Turvey, S. T., and J. H. Cooper. 2009. The past is another country: is evidence for prehistoric, historical and present-day extinction really comparable? Pp. 193–212 in S. T. Turvey, ed. Holocene extinctions. Oxford University Press, Oxford. Vermeij, G. J., and G. S. Herbert. 2004. Measuring relative abundance in fossil and living assemblages. Paleobiology 30:1–4. Western, D., and A. K. Behrensmeyer. 2009. Bone assemblages track animal community structure over 40 years in an African savanna ecosystem. Science 324:1061–1064. Wignall, P. B., and M. J. Benton. 1999. Lazarus taxa and fossil abundance at times of biotic crisis. Journal of the Geological Society, London 156:453–456. Worthy, T. H., and R. N. Holdaway. 2002. The lost world of the moa. Indiana University Press, Bloomington. Zeuner, F. E. 1963. A history of domesticated animals. Hutchinson, London. Zheng, B., and A. Agresti. 2000. Summarizing the predictive power of a generalized linear model. Statistics in Medicine 19:1771–1781.