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Late Cretaceous Restructuring of Terrestrial Communities Facilitated the End-Cretaceous Mass Extinction in North America

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Late Cretaceous Restructuring of Terrestrial Communities Facilitated the End-Cretaceous Mass Extinction in North America Late Cretaceous restructuring of terrestrial communities facilitated the end-Cretaceous mass extinction in North America Jonathan S. Mitchella,b, Peter D. Roopnarinec, and Kenneth D. Angielczyka,b aCommittee on Evolutionary Biology, University of Chicago, Chicago, IL 60637; bDepartment of Geology, Field Museum of Natural History, Chicago, IL, 60605; and cDepartment of Invertebrate Zoology and Geology, California Academy of Sciences, San Francisco, CA 94118 Edited by David E. Fastovsky, University of Rhode Island, Kingston, RI, and accepted by the Editorial Board September 21, 2012 (received for review February 6, 2012) The sudden environmental catastrophe in the wake of the end- Maastrichtian communities to test whether disturbances could Cretaceous asteroid impact had drastic effects that rippled through cause extinctions more easily in Maastrichtian communities than animal communities. To explore how these effects may have been earlier Campanian ones by using a food-web model, cascading exacerbated by prior ecological changes, we used a food-web extinctions on graphs (CEG) (12, 13, 15), that is specifically model to simulate the effects of primary productivity disruptions, designed to accommodate the uncertainties of fossil data. We such as those predicted to result from an asteroid impact, on ten chose 17 well-sampled Late Cretaceous locations (22–95 taxa Campanian and seven Maastrichtian terrestrial localities in North each; SI Materials and Methods) and nine formations, and sub- America. Our analysis documents that a shift in trophic structure jected a total of 2,600 species-level food webs drawn randomly between Campanian and Maastrichtian communities in North from the entire pool of potential webs to varying primary pro- America led Maastrichtian communities to experience more second- ductivity disruptions (see Materials and Methods, and SI Materials ary extinction at lower levels of primary production shutdown and and Methods for details; Fig. 1A shows the pattern of secondary possess a lower collapse threshold than Campanian communities. extinction at varying perturbation levels for 100 food webs at a Of particular note is the fact that changes in dinosaur richness had single example site. Fig. 1B compares the median secondary a negative impact on the robustness of Maastrichtian ecosystems extinction patterns for all 17 sites; see SI Materials and Methods against environmental perturbations. Therefore, earlier ecological for complete secondary extinction at each site). By focusing on restructuring may have exacerbated the impact and severity of the locations and formations that are exceptionally rich and well- end-Cretaceous extinction, at least in North America. sampled, we mitigated some of the biases that often plague paleobiological investigations. dinosaur diversity | extinction selectivity | paleoecology | trophic cascade | Many current macroevolutionary hypotheses are tested through cascading extinctions on graphs the use of richness curves, diversification rates, or patterns of disparity, yet regularly postulate ecological scenarios specificto EVOLUTION he end-Cretaceous mass extinction was a pivotal event in those hypotheses. Our goal is to assess macroevolutionary patterns TEarth history with effects still observable today (1). As the by using well-established ecological and evolutionary principles only major mass extinction with a well-supported ultimate cause that underlie all historical scenarios, regardless of historical (2, 3), the end Cretaceous has received intense scrutiny. How- contingencies (6). However, understanding ecosystem dynamics ever, why this impact resulted in a mass extinction and other in deep time requires a more inferential approach than is used significant abiotic events sometimes did not (4), and why some in studies of extant communities where interactions can be ob- clades and ecological guilds suffered more than others, remain served directly (16). Our method uses uniform assumptions based open questions. We reconstructed Late Cretaceous terrestrial on measures of modern food-web topology such as how links are distributed between taxa, or how productivity scales with herbi- EARTH, ATMOSPHERIC, food webs from North America to determine whether changes in AND PLANETARY SCIENCES community structure, including apparent declines in nonavian vore richness, creating model outputs that differ solely as a result dinosaur richness during the Late Cretaceous, may have made of the input data, rather than assumptions of different ecological these communities more prone to cataclysmic extinction. How functioning at different times. A major advantage of explicit richness is divided among functional groups (guilds) in a com- models such as CEG is that all assumptions about mechanisms munity influences the propagation of perturbations through a and parameters are laid bare, rendering them far more open to direct testing than verbal models. community and how those perturbations cause extinction (5). The terrestrial record of North America is the best sampled Dynamic changes to the relative richness of different guilds can and most often studied portion of the global Late-Cretaceous occur both by evolution on long time scales and community as- terrestrial record (17, 18). However, reliance on North America sembly on ecological time scales (6). Therefore, if ecosystem to understand global patterns has produced arguments for a restructuring is found to be widespread and/or frequent, it may more gradual, less catastrophic decline of dinosaurs at the end of help explain why it is so hard to predict mass-extinction survi- the Cretaceous (19, 20). This debate over the tempo and mode of vorship based on previous background extinction rates (7). nonavian dinosaur extinction traditionally focused on trajectories Food-web models have been used previously to explore and simulate how the structures of modern (8–10) and ancient (11–13) ecosystems influence their responses to perturbations. The end- Author contributions: J.S.M., P.D.R., and K.D.A. designed research; J.S.M., P.D.R., and K.D.A. Cretaceous mass extinction is an ideal candidate for study be- performed research; J.S.M. and P.D.R. contributed new reagents/analytic tools; J.S.M., P.D.R., cause one of the proximate causes of the extinction [cessation or and K.D.A. analyzed data; and J.S.M., P.D.R., and K.D.A. wrote the paper. extreme disruption of terrestrial primary productivity (14)] is The authors declare no conflict of interest. readily assessed via simulations. Further, the North American This article is a PNAS Direct Submission. D.E.F. is a guest editor invited by the Editorial terrestrial record includes numerous, well-sampled localities Board. that are amenable to the use of food-web analysis for exploring 1To whom correspondence should be addressed. E-mail: [email protected]. hotly debated questions concerning the tempo and mode of com- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. munity change. We compared the robustness of Campanian and 1073/pnas.1202196109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1202196109 PNAS | November 13, 2012 | vol. 109 | no. 46 | 18857–18861 Downloaded by guest on September 30, 2021 AB CD Fig. 1. (A) Primary productivity perturbation versus secondary extinction for 100 species-level networks generated for the Bone Butte Quarry (see SI Materials and Methods for other locations), with the threshold perturbation marked by the red line. (B) Median secondary extinction at each perturbation for the Campanian (blue) and Maastrichtian (red) sites. (C and D) Boxplots showing the range of variation in PC1 (C) and PC2 (D) for species-level networks at each of the 17 sites, ordered by decreasing sample size, with the pooled median values for each stage represented by the red (Maastrichtian) and blue (Campanian) dashed lines. Community robustness decreases with increasing PC scores for both components. Locality abbreviations are explained in Table S1. of dinosaur richness through time (21–24). Recent work has threshold; whereas, high values on the second PC (19% of the shifted from concerns specifically about nonavian dinosaur rich- variance) corresponded to low perturbation values for the ness to potential causes of the apparent decline, particularly the collapse threshold. These components are therefore complemen- importance of geological biases and tectonic influences on rich- tary measures of community robustness, with high scores of a ness and the fidelity of the fossil record (17, 25). CEG provides community on either component representing food-web topolo- an ideal vehicle to test for a relationship between apparent dif- gies prone to extinction at low perturbation levels. Maastrichtian ferences in dinosaur richness and possible changes in ecosystem food webs are overall less robust than Campanian ones (Kolmo- structure in North America. gorov–Smirnov test, P < 0.001 for both PC1 and PC2), although there is considerable within-site variation stemming from in- Results and Discussion herent uncertainty in the fossil webs (Fig. 1A), and between-site Our results support pronounced differences in the dynamics of variation based on differences in taxonomic composition (Fig. 1 Campanian and Maastrichtian communities at the sites exam- B–D) and guild richness (SI Materials and Methods). Neverthe- ined, with markedly less robust communities in the Maastrichtian less, both nested MANOVA of PC scores using stage and site as given uniform assumptions of several ecological parameters
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