Low Beta Diversity of Maastrichtian Dinosaurs of North America

Low beta diversity of Maastrichtian dinosaurs of North America

Matthew J. Vavrek1 and Hans C. E. Larsson

Redpath Museum, McGill University, Montreal, QC, Canada H3A 2K6

Edited by David Weishampel, Johns Hopkins University, and accepted by the Editorial Board March 19, 2010 (received for review November 30, 2009) Beta diversity is an important component of large-scale patterns of zone; and an interior Triceratops zone (7,8). The boundaries ofthese biodiversity, but its explicit examination is more difficult than that three regions have been slightly modified as more fossils have been of alpha diversity. Only recently have data sets large enough been found, and later studies incorporated these new dinosaur as well as presented to begin assessing global patterns of species turnover, previous pterosaur (Quetzalcoatlus) finds (8). especially in the fossil record. We present here an analysis of beta The hypothesized provincial delineations lead to the prediction diversity of a Maastrichtian (71–65 million years old) assemblage of that beta diversity for this region as a whole should be relatively dinosaurs from the Western Interior of North America, a region that high. However, previous work was based on the occurrence of a covers ≈1.5 × 106 km2, borders an epicontinental sea, and spans few well-known individual genera that have well-defined geo- ≈20° of latitude. Previous qualitative analyses have suggested graphic boundaries within relatively small spatial scales. Such high regional groupings of these dinosaurs and generally concluded that levels of endemism would be unprecedented for any modern large- there were multiple distinct faunal regions. However, these studies bodied terrestrial fauna. did not directly account for sampling bias, which may artificially We use modern approaches to search for statistical support for decrease similarity and increase turnover between regions. Our areas ofhigh endemism. These approaches included rarefaction and analysis used abundance-based data to account for sampling inten- species estimators to calculate beta diversity and minimum spanning sity and was unable to support any hypothesis of multiple distinct trees (MST) and nonmetric multidimensional scaling (NMDS) to faunas; earlier hypothesized faunal delineations were likely a sam- search for readily apparent provinces (see Materials and Methods for pling artifact. Our results indicate a low beta diversity and support a full explanation). If there are strongly delineated provinces present, single dinosaur community within the entire Western Interior we predict that beta diversity for the Maastrichtian Western Interior region of latest Cretaceous North America. Homogeneous environ- dinosaur fauna is high and that the NMDS/MST ordination will be ments are a known driver of low modern beta diversities, and the fragmented into discrete clusters of sites. warm equable climate of the late Cretaceous modulated by the epi- contenental seaway is inferred to be an underlying influence on the Results low beta diversity of this ancient ecosystem. Using observed values of generic richness, with alpha diversity calculated from the average richness of all formations (n ¼ 24; α ¼ 5:46), biogeography | macroecology | paleoecology | Cretaceous beta diversity is relatively high at βH1 = 8.24 (Table 1). This corrob- orates the high endemism found by previous workers but takes no lpha diversity is defined by Whittaker (1, 2) as species richness account of sampling effects. There is an obvious and unsurprising on the local or habitat scale, and beta diversity is defined as the correlation between generic richness and sample size for this dataset A R2 P << difference in the types of species found in different areas of alpha ( = 0.79, 0.001; Fig. S1), illustrating the bias of differential diversity. Alpha and beta diversity together make up species sampling intensity. Only 11 of the 24 formations have more than 10 richness at the landscape scale, called gamma diversity. Because specimens recorded, and thus low alpha diversities are due to insuf- ficient sample sizes rather than actual conditions. This range of sam- beta diversity measures turnover across an area, it is closely related ECOLOGY to the numbers of endemic species within each community, which pling intensity causes beta diversity estimates to be higher than those in turn can be used to assess biotic provinciality. Quantitative obtained from evenly, well-sampled data (5). estimates of modern beta diversity recover surprisingly low beta To reduce this bias when calculating the average alpha diversity, diversity values despite broad taxonomic and geographic sampling, we eliminated all formations with fewer than 100 specimens. This regardless of the motility of the group in question (3–5). Instead, eliminated all but four formations, namely Hell Creek (Montana), beta diversity seems most correlated with climate evenness (4–6). Hell Creek (North Dakota), Horseshoe Canyon (Alberta), and We present beta diversity estimates for an ancient terrestrial Lance (Wyoming). Formations with more than 100 specimens are ecosystem. The Western Interior of North America is perhaps the expected to give the most robust values of actual alpha diversity most intensely sampled dinosaur-bearing region in the world (7). and are therefore more informative than keeping formations with fewer specimens. We believed that using only formations with The terrestrially deposited rock sequence comprises sparsely more than 100 specimens was an appropriate compromise, main- exposed Aptian (121–112 Ma) formations to extensively exposed taining high numbers of specimens while retaining enough local- Maastrichtian (71–65 Ma) formations. These Maastrichian rocks ities for reasonable estimates. Average alpha diversity uncorrected are largely floodplain deposits along the western shores of the epi- for sampling bias (Sobs) for these four localities was 13.5. However, continental Western Interior Seaway (Fig. 1). The rich Maas- for the estimates of gamma diversity, we retained all formations for trichtian deposits have been a focus of research on patterns of dinosaur distributions and biogeography on a subcontinental scale (7–13). We used this dinosaur assemblage for our analysis of beta Author contributions: M.J.V. designed research; M.J.V. performed research; M.J.V. contrib- diversity in the fossil record because it is currently the only data set uted new reagents/analytic tools; M.J.V. and H.C.E.L. analyzed data; and M.J.V. and H.C.E.L. large enough and the only region with extensive previous work on wrote the paper. endemism and provinciality. Previous studies have concentrated on The authors declare no conflict of interest. dinosaur faunal provinciality at local scales on the basis of presence/ This article is a PNAS Direct Submission. D.W. is a guest editor invited by the absence data. Specifically, these analyses have suggested high levels Editorial Board. of endemism at local, formational scales (13). The most widely 1To whom correspondence should be addressed. E-mail: [email protected]. accepted community hypothesis divides the dinosaur fauna into This article contains supporting information online at www.pnas.org/cgi/content/full/ three zones: a northern Leptoceratops zone; a southern Alamosaurus 0913645107/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.0913645107 PNAS | May 4, 2010 | vol. 107 | no. 18 | 8265–8268 Downloaded by guest on September 27, 2021 Table 1. Results for rarefaction and alternate methods of species estimation for the highlighted formations and full region Locality No. of specimens Generic richness (observed) Rarefaction Chao 1 ACE Jackknife 1 Average estimated richness*

Hell Creek Montana 211 17 14.38 19.58 15.66 18.2 17.81 Hell Creek North Dakota 268 9 6.68 8.5 10.15 8.58 9.08 Horseshoe Canyon Alberta 120 14 12.85 28.99 14.94 18.73 20.88 Lance Wyoming 111 14 13.88 14.58 14.35 15.39 14.77 Average α† 177.5 13.5 11.95 17.91 13.77 15.22 15.64 ‡ Western Interior 997 45 21.95 40.55 28.02 31.72 33.43

βH1 — 3.33 1.84 2.26 2.03 2.08 2.14

*Average estimated richness is the mean value of Chao 1, ACE, and Jacknife 1. † Values for the average α were calculated using only the four listed formations. ‡Values for the entire Western Interior region were calculated using all 24 localities from the dataset.

the calculation. This method would likely overestimate gamma When beta diversity was recalculated with an average alpha diversity, because there were many genera known for this region diversity calculated from only the four formations mentioned that have not been found within these four formations. above, beta diversity dropped greatly to βH1 = 3.33. However, the sampling intensities for each formation and the region in total vary greatly, from n = 111 (Lance Wyoming) to n = 268 (Hell Creek North Dakota). Rarefaction methods were used to compensate for these large differences (Fig. 2). After all samples were rareﬁed, generic richness for each formation dropped com- paratively little (α ¼ 11:95), whereas gamma diversity decreased by nearly half. Consequently, beta diversity also showed a large decrease to βH1 = 1.84. One criticism of rarefaction is that, although accounting for sample size, it does not reﬂect different rates of increase in species richness due to differences in underlying species evenness (14, 15).

Total Hell Creek Montana Hell Creek North Dakota Horseshoe Canyon Alberta Lance Wyoming 10 15 20 25 30 35

05 A B Species Richness (S)

Fig. 1. Approximate locations of Maastrichtian-aged dinosaur-bearing formations from the Western Interior of North America used in this analysis. (A) Abbreviations of formation names are as follows: A, Aguja; D, Denver; Fe, Ferris;

0 5 10 15 20 25 30 35 C D Fr, Frenchman; HM, Hell Creek Montana; HN, Hell Creek North Dakota; HS, Hell Creek South Dakota; HC, Horsehshoe Canyon; J, Javelina; Kp, Kaiparowits; Kd, 0 204060801000 20 40 60 80 100 Kirtland; LM, Lance Montana;LS, Lance South Dakota; LU, Lance Utah;LW, Lance Number of Individuals (N) Wyoming; LaC, Laramie Colorado; Law, Laramie Wyoming; M, McRae; N, North Horn; P, Pinyon Conglomerate; Sc, Scollard; SA, St. Mary’sRiverAlberta;SM,St. Fig. 2. Comparison of methods of sample size correction. (A) Smoothed Mary’s River Montana; T, Tornillo Texas. (B) Locations of occurrences of the three curves for rarefaction using Coleman’s random placement method, up to n = indicator taxa, Alamosaurus (A), Leptoceratops (L), and Triceratops (T). Greyed 100. (B) Smoothed curves for Chao 1 values up to n = 100. (C) ACE values. (D) area to the east is the approximate location of the inland seaway. Jacknife 1 values.

8266 | www.pnas.org/cgi/doi/10.1073/pnas.0913645107 Vavrek and Larsson Downloaded by guest on September 27, 2021 For example, an area with high species evenness will show a faster Discussion rate of increase than an area with a low evenness, because of very We find no evidence to support distinct faunal regions of dino- rare species taking much longer to be found. A way to compensate saurs during the Maastrichtian stage of the Western Interior of for this problem is by extrapolating to an estimate of total species North America. Although our estimates of beta diversity are richness, using species estimators. much lower than what might be expected from direct observation Nonparametric estimators, although designed to be independent of the fossil record, the effect of uneven sampling can be very of sample size, are still affected by sampling to some extent. To correct large. When sampling the richness of a region, one should not for this, we ran estimators 1,000 times on a randomized subsample expect to find all of the species present, with rare species often from each locality with more than 100 specimens. Although the not detected even in large samples (16). estimated richness from the three methods differed considerably, the Another possible explanation for low beta diversity might be the overall result was a higher estimated alpha diversity (α ¼ 15:64) and a time scale used. Studies on modern community associations are lower βH1 value. The Chao 1, abundance-based coverage estimator limited to relatively brief periods of sampling time. Moreover, the (ACE), and Jacknife 1 estimations yielded beta diversities of 2.26, Maastrichtian stage represents approximately 6 million years, and 2.03, and 2.08, respectively. time averaging effects are undoubtedly confounding the data. Work Finally, NMDS networks offer a test of similarity between all on shorter time scales during the Pleistocene epoch has shown that sites. If there were three distinct provinces as hypothesized, there mammal species move independently, reorganizing community would be at least three discrete clusters of sites within the net- compositions in time scales of only 350,000 years (17, 18). Even the work. If each individual site has large numbers of endemic taxa, large faunal exchange between North and South American mam- the NMDS would show overdispersal, with all sites plotting in a mals during the Great American Interchange occurred over ≈3 ring to maximize site-to-site dissimilarities. The NMDS network million years, with continental-scale migrations of mammals from plot is significantly different from either of these possibilities shrews to mastodonts (19). Although the climate of the Late Cre- (Fig. 3B). Sites are scattered evenly throughout the plot space, taceous was more stable than that of the Holocene epoch, the and no clusters are present, with little patterning in regard to suggestion that large, motile animals might maintain cohesive units endemism. The same network plotted on geographic space (Fig. seems unlikely. 3A) emphasizes the lack of regional clusters. In general, dinosaur Harrison et al. (3) obtained beta diversity levels in British birds β faunal similarity between sites is poorly associated with geo- between H1 = 3.3 and 5.7, higher levels than we calculated here β ¼ : graphic distance (Fig. 3C), because pairwise values of generic ( H1 2 14) and over a much smaller latitudinal range. Our results similarity show little decay over distance. indicate less turnover across a greater distance and add further evidence for a lack of dinosaurian endemism and provinciality during the Maastrichtian stage along the Western Interior Seaway. Novotny et al. (5) present a lower beta diversity for tropical insects than we found for dinosaurs, noting that their study sampled a relatively climatically homogeneous landscape. One possible implica- tion is that the low levels of beta diversity within Maastrichtian dinosaurs are due to climactic factors. During the latest Cretaceous epoch the global climate was much warmer, with more equable temperatures and a greatly reduced latitudinal temperature gradient (20, 21). The average yearly temperature at the equator for the Maastrichtian stage has been suggested to be only slightly warmer than it is today, whereas polar regions were estimated to have been B 15–25 °C higher than they are today, with mean temperatures for the

coldest months likely above freezing (21). ECOLOGY Although this analysis does not support distinct communities of dinosaurs, some dinosaurs probably were restricted in their ranges. For example, the sauropod Alamosaurus likely did not live in the northern-most regions of the Western Interior region. This taxon has not been recovered north of Utah despite its large size and conspicuousness. However, it seems counterintuitive that an ani- mal as large as Alamosaurus would not have dispersed at low levels to regions other than the restricted area it is found over its several C million year existence. Modern species ranges often have one or more high-density peaks, where the species is highly abundant, and A tails, where the species can still be found but at very low densities (22). The fossil record of Alamosaurus likely shows these high- density regions, and because of random chance, individuals that Fig. 3. Relative pairwise similarities between localities. (A) Map of the may have lived in the low-density regions of their ranges are simply localities used in the analysis with an MST added to indicate the relative not preserved. Therefore, although we may be seeing signatures of similarities between localities. The more similar two localities are to one generic and species ranges within the fossil record, we are by no another on the basis of the species present, the darker the line connecting means seeing the entire region in which they lived. Rather than them will be. Note that no clusters are formed, and many localities are more faunal provinces per se, previous research has likely recovered similar to far-ranging ones than neighboring localities. (B) Plot of the rela- these high-density areas for specific taxa. tive positions of an NMDS of the localities, showing no apparent clusters. (C) Our results suggest that any one region of the Western North Pairwise dissimilarity of sites in comparison with their geographic distance American Seaway would have had much higher dinosaur generic from one another. As dissimilarity increases, the sites are interpreted to be less similar to one another. The line represents a locally weighted sum of richness than that observed, with approximately 16 genera of squares function. The sites show a slight decay over distance, although a dinosaur on average. At the continental scale, levels of beta linear regression is not significantly different from 0. These graphs indicate diversity among dinosaur assemblages are comparable to modern low beta diversities for this assemblage. Abbreviations as defined in Fig. 1. terrestrial faunas with low endemicity. These results suggest that

Vavrek and Larsson PNAS | May 4, 2010 | vol. 107 | no. 18 | 8267 Downloaded by guest on September 27, 2021 dinosaurs were not as restricted in their ranges as once thought and r ¼ αβ that the fauna as a whole was largely homogeneous. Materials and Methods By rearranging this relationship, Whittaker (24) originally defined beta diversity as γ This study hasmade use ofrecent developmentsin theextensivecataloguingof β ¼ dinosaurremainsattheonlineandopenPaleobiologyDatabase(PaleoDB.org). W α All location and abundance data were downloaded from the Paleobiology Database on January 14, 2009, using the taxon name ”Dinosauria” and a time Althoughthemeasureisuseful,itsinterpretationattimescanbeconfusing.Because span of “Campanian” to ”Maastrichtian,” with the following parameters: of the way it is calculated, the minimum value (complete similarity) is 1, whereas Continent = “North America”; Abundance Value = TRUE; State = TRUE; and the maximum value (complete dissimilarity) is equal to the number of regions of Formations = TRUE. The majority of this data set originated from the work of alpha diversity used. Instead, Harrison et al. (3) suggested the modification Carrano (23) to collect and collate the record of Dinosauria throughout the fi γ Mesozoic era. The downloaded data were further ltered manually in − 1 OpenOffice.org Calc to exclude any taxon unidentifiable to genus. All avian β ¼ α ; H1 taxa were excluded, and Mexican and Alaskan faunas were removed to keep ðN − 1Þ × 100 our data more comparable to previous work. Generic-level identifications were used for the same reason. As well, most dinosaur genera of this age are whichthengivesamoreintuitivevaluebetween0and100,with0beingcomplete monospecific, so this more coarse taxonomic rank still accurately reflects our similarity and 100 complete dissimilarity between sites. Although many other understanding of dinosaur species-level diversity. Formations were divided up methods ofcalculatingbetadiversity havebeensuggested, Whittaker’smeasure by state and province, approximating the divisions of Lehman (7). However, has remained one of the simplest and most commonly used (14). we found similar results when formations were not divided by state. In Data analysis and all figures were done using the R Statistical package (25), determining values of species richness for the entire data set, all formations for with the packages ecodist (26), fossil (27), PBSmapping (28), proj4 (29), and which at least one genus with available abundance data was present were shapefiles (30). For each formation, randomizations were run 1,000 times. used. Dinosaur fossil records for many individual formations were too frag- Rather than true rarefaction, Coleman curves were calculated, using Cole- mentary to be used in an analysis of this type. To have adequate sample sizes man’s “random placement” method, which provides results virtually indis- for the rarefaction and species estimation, we used only sets that had more tinguishable from rarefaction but is computationally much simpler (14, 31– than 100 specimens, limiting us to four assemblages. Addtionally, although 33). Values reported for species estimators are the statistical average, cal- there were two cases of bonebeds included, these were eliminated because of culated from 1,000 randomizations. For the species estimators, values are their confounding effects on the various statistical methods. Although records from estimates calculated at n = 100. The estimates were calculated at this include both instances of specimens and individuals, representing isolated level to compensate for any bias from sampling intensity. For the full data elements and relatively complete skeletons, respectively, we did not differ- tables and R code used for the analysis and figure generation, please consult entiate so as to retain as much data as possible. Absolute values for species Datasets S1 and S2 and SI Appendices S1 and S2. diversity were lower when analyses were run with only specimen records, although beta diversity values were nearly unchanged (Table S1). ACKNOWLEDGMENTS. We thank Meaghan A. Vavrek for assistance with Diversity can be partitioned into different components at different levels fi manuscript preparation; and two anonymous reviewers for comments on of scale. Whittaker (1, 2) de ned alpha diversity as species richness on the the manuscript. Funding for this project was provided by a National Sciences local or habitat scale, with beta diversity as the differences between areas of and Engineering Research Council Canada Graduate Scholarship (PhD) (to M. alpha diversity. Together, alpha and beta make up gamma diversity, or J.V.), a Canada Research Chair (to H.C.E.L.), and by National Sciences and species richness at the landscape scale. Engineering Research Council Discovery Grant 204548 (to H.C.E.L.).

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8268 | www.pnas.org/cgi/doi/10.1073/pnas.0913645107 Vavrek and Larsson Downloaded by guest on September 27, 2021