Climate Directly Influences Eocene Mammal Faunal Dynamics in North America

Climate directly influences Eocene mammal faunal dynamics in North America

Michael O. Woodburnea,1, Gregg F. Gunnellb, and Richard K. Stuckyc

aDepartment of Geology, Museum of Northern Arizona, Flagstaff, AZ 86001; bMuseum of Paleontology, University of Michigan, Ann Arbor, MI 48109; and cDenver Museum of Nature and Science, Denver, CO 80205

Communicated by W. A. Berggren, Woods Hole Oceanographic Institution, Woods Hole, MA, June 19, 2009 (received for review December 18, 2008) The modern effect of climate on plants and animals is well docu- in the later Bridgerian (the BC). The BC was driven by a strong mented. Some have cautioned against assigning climate a direct retreat from tropical climates to the increased seasonality and role in Cenozoic land mammal faunal changes. We illustrate 3 overall aridity that characterized the later part of the Eocene in episodes of significant mammalian reorganization in the Eocene of North America (Fig. 1). In the following text, we summarize the North America that are considered direct responses to dramatic climatic and faunal events embodied within the PETM, EECO, climatic events. The first episode occurred during the Paleocene– and BC, provide a brief comment on the hiatus in climatic and Eocene Thermal Maximum (PETM), beginning the Eocene (55.8 Ma), faunal change between the PETM and EECO, and conclude with and earliest Wasatchian North American Land Mammal Age a discussion of these results. (NALMA). The PETM documents a short (<170 k.y.) global temperature increase of Ϸ5 °C and a substantial increase in first appear- The PETM Immigration Stimulus ances of mammals traced to climate-induced immigration. A 4-m.y. The PETM has been well studied and documented (3–14). In period of climatic and evolutionary stasis then ensued. The second continental records from the western U.S., a temperature spike climate episode, the late early Eocene Climatic Optimum (EECO, (to Ϸ20–25 °C) has been shown to occur simultaneously with the 53–50 Ma), is marked by a temperature increase to the highest earliest Eocene mammalian faunas (Wa-0), coincidental with a prolonged Cenozoic ocean temperature and a similarly distinctive sharp interval of mammalian immigration (4, 15). Climate

continental interior mean annual temperature (MAT) of 23 °C. This changed strongly, but plant diversity did not, except briefly GEOLOGY MAT increase [and of mean annual precipitation (MAP) to 150 during the PETM (8). cm/y) promoted a major increase in ﬂoral diversity and habitat Immigrants at the beginning of the Wasatchian (Wa-0) in- complexity under temporally unique, moist, paratropical condi- cluded hyaenodontid creodonts, true primates, artiodactyls, and tions. Subsequent climatic deterioration in a third interval, from 50 perissodactyls (4). The immigrant and other new taxa comprise to 47 Ma, resulted in major faunal diversity loss at both continental a major increase of 9 genera relative to the late Paleocene [Cf-3, and local scales. In this Bridgerian Crash, relative abundance Fig. 1; Table 1, and supporting information (SI) Table S1]. shifted from very diverse, evenly represented, communities to Wa-0 reflected a distinct peak in browsing herbivores and

those dominated by the condylarth Hyopsodus. Rather than being terrestrial taxa, along with a sharp drop in insectivores (16). EVOLUTION ‘‘optimum,’’ the EECO began the greatest episode of faunal turn- Whereas phenacodontid condylarths and plesiadapid primates over of the ﬁrst 15 m.y. of the Cenozoic. were the major herbivores in the late Clarkforkian (Cf-3), in the Wasatchian, these taxa were replaced by more terrestrial and Bridgerian Crash ͉ climate change ͉ EECO ͉ faunal change ͉ herbivorous/frugivorous forms, such as hyopsodontid condy- mammal faunas larths, equid perissodactyls, and dichobunid artiodactyls (17). Similarly, some viverravids, and large creodonts (oxyaenids) were the major carnivores in the late Clarkforkian, versus a rising hereas the effect of climate on modern biota is well importance of miacids, hyaenodontids, and additional oxyaenids understood, assigning climate a direct role in Cenozoic W in the Wasatchian. Dwarfing of certain lineages (Ectocion, land mammal faunal changes has been questioned (1). Evidence Copecion, Hyracotherium, Prodiacodon, Macrocranion, Leptac- presented here indicates that the Paleocene–Eocene Thermal odon, Wyonycteris, Niptomomys, and Uintacyon) is another dis- Maximum (PETM), the Early Eocene Climatic Optimum tinct innovation in Wa-0 faunas (3, 18, 19) also attributed to (EECO), and the Bridgerian Crash (BC) reflect distinct episodes climatic modification. of Eocene climate change in North America. Each has a different The PETM is considered to have abetted intra- and intercon- impact on mammalian faunas of the interior of North America, tinental dispersal of plants and land mammals (3, 20, 21). Tiffney at 55.8 Ma (2), 53–50 Ma, and 50–47 Ma, respectively (Fig. 1). (20) characterized the high-latitude flora as consisting of warm Global ocean temperature, U.S. western interior mean annual temperate-to-subtropical-adapted taxa that survived a mean temperature (MAT), mean annual precipitation (MAP) and coldest month temperature of Ϸ10 °C. North American mammalian diversity are shown in Fig. 1. Fig. Immigration played a strong role in affecting Wa-0 faunal 1 provides citations to the paleobotanical records that demon- dynamics, the impetus of which seems to have carried over into strate the climate changes associated with MAT. Ͻ subsequent biochrons of the Wasatchian. Wa-1 shows a strong The PETM occurred over a short interval of time ( 170 ky) rise in numbers of taxa (96; Fig. 1) and a large number of FADs at the beginning of the Wasatchian North American Land (27% of the total fauna, Fig. 2), versus very few LADs (2%, Mammal Age (NALMA), when the abrupt warming of northern Table 1), and no immigrants. Immigrants account for Ϸ43% of Hemisphere climate stimulated a strong pulse of mammalian the FADs in Wa-0 (Fig. 2 and Table 1) in contrast to the situation immigration to North America and dwarfing within some lineages (3, 4) and cladogenesis within others (1). The EECO (late Wasatchian and early Bridgerian NALMAs; Fig. 1) witnessed a Author contributions: M.O.W. designed research; M.O.W., G.F.G., and R.K.S. performed stronger overall increase in tropicality as well as floral diversity research; M.O.W., G.F.G., and R.K.S. analyzed data; and M.O.W. wrote the paper. compared with the PETM. This resulted in a major impact on The authors declare no conﬂict of interest. mammalian faunal dynamics and increased diversity in the 1To whom correspondence should be addressed. E-mail: [email protected]. absence of any major stimulus from immigration. Subsequently, This article contains supporting information online at www.pnas.org/cgi/content/full/ there was an extensive reduction in faunal balance and diversity 0906802106/DCSupplemental.

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0906802106 PNAS ͉ August 11, 2009 ͉ vol. 106 ͉ no. 32 ͉ 13399–13403 Downloaded by guest on October 1, 2021 Fig. 1. Summary of temperature, rainfall, and mammalian diversity for the Western Interior of North America. Sea surface temperatures rise gradually from the Late Cretaceous into the early Eocene and then decline toward the late Eocene. The megafloral record responds in a generally similar way at least from the late Paleocene to the late Eocene, with a strong transient excursion at the PETM and a similarly warm interval during the EECO from Ϸ53 to 50 Ma. During the EECO, mean annual rainfall gradually decreased from Ϸ150 cm/y to 100 cm/y. From Ϸ50 Ma, both MAT and MAP, as well as tropicality, decrease sharply, to cooler, drier, and more open conditions. The mammalian diversity pattern generally reflects the MAT record, except that the PETM spike promoted immigration rather than in situ diversification in contrast to the opposite response during the EECO. Sources are cited in the figure.

in Wa-1. The immigration stimulus of Wa-0 resulted in vigorous (22% and 25%, respectively), a strong advance over the levels in speciation in Wa-1 that accounts for the greatest single numer- Wa-6 (Fig. 2). Lambdotherium (a perissodactyl) appears to have ical increase of any biochron from the late Tiffanian through the been the only immigrant. Wa-7 witnessed a major faunal reor- Uintan (Fig. 1 and Table 1). It is additionally remarkable that the ganization. Chief innovations appear to be an increased diversity Wa-1 increase in taxa took place over a span of Ϸ0.2 Ma (2). In of rodents, primates, artiodactyls, and perissodactyls (Table S1). contrast, comparable (but still smaller) increases in taxa took The wet and subtropical conditions in Wa-7, the 87% plant place within an interval of Ϸ3.7 m.y. (Wa-5–Br-1a) or Ϸ8 m.y. species turnover relative to those of the Paleocene (13), and (Br-3–Ui-3; Fig. 1). the great floral diversity of the time, apparently is reflected by the increase in mammalian diversity from Wa-6 (Fig. 1) Medial Wasatchian Stasis despite the LADs portrayed in Fig. 2. Subsequent to the PETM, a period of stasis is recorded in the medial Wasatchian. Figs. 1–3 and Table 1 indicate that the Wa-2– The Bridgerian Expansion Wa-5 interval witnessed a drop in taxonomic diversity subsequent The EECO witnessed a major expansion in the Bridgerian, which to Wa-1 and a relative dearth of FADs and LADs. Mammals lived began with a significant episode of new evolutionary diversifi- under a climate that became cooler and seasonally drier than during cation (104 genera in Br-1a; Fig. 1 and Table 1), with FADs and just after the PETM. There were no immigrants, and phyletic (29%) far outnumbering LADs (13%) (Fig. 2). The 30 FADs is innovations were basically unremarkable. the largest number of any biochron from Cf-1 to the Uintan EECO Initial Diversification (Table 1). Although some losses occurred in Br-1a, the main pattern was origination and diversification under a wet parat- This pattern changed dramatically during the EECO, which began in the late middle Wasatchian (Wa-6; Figs. 1–3), and is ropical climate. The brontothere Eotitanops, the rhino-like Hyra- reflected in an increase in diversity (92 taxa; Fig. 2 and Table 1). chyus, and the tillodont Trogosus may be immigrants in Br-1a; There are few immigrants (the tapiroid Heptodon being one of however, they apparently had little effect on subsequent faunal the likely possibilities). The interval records new rodents, eupri- diversity. mates, pholidotans, and a possible dermopteran of North Amer- Before the Bridgerian, anaptomorphines were the dominant ican origin (Table S2). The higher number of FADs in Wa-6 omomyid euprimates (in both abundance and diversity), first indicates an increase in speciation rate and thus the total number appearing in Wa-0, diversifying shortly thereafter, and main- of taxa over those of Wa-5 (Fig. 1 and Table 1), despite a taining fairly consistent diversity through the Wasatchian and proportionately greater percentage of LADs than FADs in Wa-6 early Bridgerian, until they began to diminish in the later (Fig. 2) and the strong increase in LADs relative to those of Bridgerian and Uintan. Omomyine euprimates first appear in Wa-5. The strength of cladogenesis in Wa-6 is greater than would Wa-4 and were as diverse as anaptomorphines but became more be implied by its net increase in total taxa alone. abundant by Br-1a, where they began a major proliferation that Wa-7 continues the increase in mammalian diversity (to 98 continued into the Uintan (22, 23). This was accompanied by a genera), and shows a high percentage of both FADs and LADs radiation of hypercarnivores, a diversity of new artiodactyls, and

Table 1. Late Paleocene and early Eocene North American immigrant mammalian genera, FADs and LADs Biochron Ti3 Ti4 Ti5 Ti6 Cf1 Cf2 Cf3 Wa0 Wa1 Wa2 Wa3 Wa4 Wa5 Wa6 Wa7 Br1a Br1b Br2 Br3 Ui1 Ui2 Ui3

Total genera 73 74 67 53 60 63 61 72 95 93 90 89 91 92 98 104 96 96 84 96 95 108 Immigrants Genera 1 0 1 1 3 1 1 9 0 0 0 0 0 0 1 ?3 0 1 4 2 1 2 Pct of FADs 8 0 14 17 38 9 25 43 0 0 0 0 0 0 5 ?10 0 7 50 5 6 6 Pct of total 1 0 1 2 5 2 2 13 0 0 0 0 0 0 1 ?3 0 1 5 2 1 2 FADs Number 13 14 7 6 8 11 4 21 25 1 2 6 9 11 22 30 6 14 8 40 18 33 Percent 18 19 10 11 13 17 7 29 26 1 2 7 10 12 22 29 6 15 10 42 19 31 LADs Number 13 15 20 1 8 6 10 2 3 5 7 7 10 16 24 14 15 20 27 19 18 42 Percent 18 20 30 2 13 10 16 3 3 5 8 8 11 17 25 13 16 21 32 20 19 39 MAT °C From Fig. 1 12 10 11 Ϸ12 14 18 17 20 Ϸ17 18 17 Ϸ16 15 17 23 Ϸ21 19 Ϸ17 16 15 – –

13400 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0906802106 Woodburne et al. Downloaded by guest on October 1, 2021 Fig. 3. Rarefaction analysis of species diversity in Eocene and early Oligocene intervals in North America. The number of specimens (x axis) is compared with the number of species in each interval (y axis). Early Wasatchian (Wa-1–5, Fig. 2. Portrayal of FADs and LADs for North American late Paleocene and squares), latest Wasatchian and earliest Bridgerian (Wa-7–Br-1a, circles), me- early Eocene mammals, based on percentage relative to total number of taxa dial Bridgerian (Br-2–gray polygons), Uintan and Duchesnean (Ui-2–Du, dia- in each biochron. Positions of PETM, EECO, and mammal biochrons, are monds), and Chadronian and Orellan (Ch–Or, triangles). Specimen counts are indicated. Selected figures for MAT and general climatic conditions follow Fig. based on individual fossiliferous horizons and are not generalized from GEOLOGY 1 and the text. The black bar indicates the percentage of immigrants for each stratigraphic intervals. Note the high levels of species diversity during the early biochron. part of the EECO that dramatically drops during the medial Bridgerian after the optimum. The figure suggests that the alpha species diversity for Wa-7– Br-1a is Ͼ1.5 times greater than during Br-2, indicating a drop in alpha the appearance of multiple lineages of brontotheriid perissodac- diversity after the early EECO that is reflective of high levels of both point tyls by the end of the Bridgerian (Table S1). diversity and continental diversity during that time. Data were derived from The greatly increased diversity is also seen in rarefaction Denver Museum of Natural Science collections for Br-2 and from Stucky (25) for the other intervals. analysis (24), based on Stucky (25), with the addition of 18 new localities of Br-2 age (Fig. 3). Faunas from Wa-7–Br-1a approx- EVOLUTION imately doubled in alpha diversity compared with those of In contrast to the relatively small number of FADs, taxonomic Wa-1–Wa-5. Alpha diversity subsequently was dramatically re- loss during the interval Br-1b–Br-3 is substantial, in part indi- duced by Ϸ40% during Br-2. The early EECO diversity increase cated by the LADs shown in Fig. 2, and the conclusion seems and its later 40% decline are coincident with the climatic and inescapable that extinctions were promoted by the coeval retreat floral patterns discussed herein. to cooler and more seasonally arid and conditions. Concomitant with the increase in overall alpha diversity in In summary, the large number and diversity of gains and then Wa-7–Br-1a, the condylarth Hyopsodus replaced the perissodac- losses and reductions in the EECO is in striking contrast with tyl Hyracotherium as the most abundant genus in some areas, virtually all other mammalian biochrons since the beginning of often representing as much as 28% of all mammalian specimens the Cenozoic Era. There were very few immigrants, so this factor (25). The early part of the EECO (Wa-6–Br-1a) was marked by was inconsequential to the FADs or the larger number of LADs a high level of insectivory, scansoriality, and arboreality (18). found in Br-1b, Br-2, and Br-3. Speciation in these biochrons In summary, the EECO is one of substantial innovation, with apparently was driven by factors other than the stimulus of very high numbers of FADs occurring from Wa-6–Br-1a (63; immigration, in distinct contrast to the situation from Wa-0 to Table 1). Wa-1. The much greater floral diversity associated with the EECO The BC also must have provided a major stimulus not present in the The BC provides a different pattern, however, apparently re- earlier Wasatchian (20, 21, 26, 27). The faunal dynamics of the EECO were much more diverse than the substantially more flecting the deterioration of the climate and coeval floras. Table regular pattern seen from Wa-2 to Wa-5. Whereas immigration 1 shows that, whereas the number of FADs is small, the number had no apparent effect in either interval, the drop in MAT in the of LADs remains substantial in Br-1b–Br3 and that the total later EECO (from Ϸ21 °C to 16 °C) was nearly twice that seen number of mammalian genera (diversity) drops significantly (104 Ϸ Ϸ in Wa-2–Wa-5 (from 18 °C to 15 °C; Table 1). Modification of to 84 genera, or 19%) from Br-1a to Br-3. habitats during this climatically drier interval also may be The interval from Br-1b to Br-3 reflects a major reorganiza- reflected in the progressive drop in total numbers of genera from tion of the fauna. FADs in Br-1b are only 6% of the fauna (now Br-1a to Br-3 (Fig. 1). at 96 genera), whereas LADs comprise 16% (Table 1). There are no immigrants or new suprageneric groups in Br-1b and only one Discussion immigrant in Br-2 (Fig. 2). In Br-2, Hyopsodus increased in The data assessed in this report show instances (medial Wa- abundance to the extent that it represented 61% of all mamma- satchian; Wa-2–Wa-5) where climate was relatively benign and lian specimens from some areas. Such dominance by a single apparently served as the basic background upon which a rela- taxon is unknown in any other mammalian biochron of the tively modest degree of faunal dynamism was developed. In this Cenozoic Era (25). case, both innovation (FADs) and extinctions/declines (LADs)

Woodburne et al. PNAS ͉ August 11, 2009 ͉ vol. 106 ͉ no. 32 ͉ 13401 Downloaded by guest on October 1, 2021 were approximately in balance, and both were at modest levels. Neither Alroy et al. (1) nor Alroy (28) specifically discuss the Immigration played only a minor role (or none at all). The basic EECO, although ‘‘the second highest net diversification value’’ is pattern of mammalian faunal dynamics indicates that the role of found in the earliest Bridgerian in ref. 1. This is not attributed to climate through most of the middle part of the Wasatchian was climate change. In fact, the interval herein discussed as pertaining inconsistent at best and likely of no major influence. to the EECO is not addressed in Alroy et al. (1) or Alroy (28). As The late Clarkforkian (the interval just preceding the Wa- indicated in Fig. 1, Br-1a records the greatest generic diversity of satchian; Fig. 1) documents an increasingly warm climate with mammalian taxa in the EECO, just before its precipitous drop to moist, subtropical conditions by Wa-0. Plant diversity decreased the end of that interval. Fig. 1 shows that Br-1a faunas lived at or notably, however, in the latest Clarkforkian and early Wasatch- just after the maximum of MAT and tropical plant diversity in the ian, indicated in part by decreases in MAT and MAP, and Western Interior. The covariance and synchrony of the plant and mammalian generic diversity fell from Cf-2 to Cf-3 (Table 1 and mammal records suggests to us a climatic cause. Fig. 1). Immigrants are important taxonomically in the Clark- In conclusion, the faunal and floral dynamics presented in this forkian (e.g., introduction of the Rodentia in Cf-1) and contrib- report support a direct climatic cause for both the EECO and the uted Ϸ5% of the new genera of the interval (Table 1). Although PETM. Despite the fact that the dynamic details differed in each climate perhaps facilitated immigrations, Clarkforkian faunal case, climate change played a major role in molding the land increase was only modest, with an actual reduction in total mammal faunas of those times. number of taxa and an increase in LADs from Cf-2 to Cf-3. The early Wasatchian (Wa-0–Wa-1) was dramatically differ- Methods ent. FADs greatly outnumber LADs in the early Wasatchian, Explanation of Terms. resulting in a great increase in generic diversity. Early Wasatch- FAD, the first stratigraphic occurrence of a taxon, considered to have been ian floras were substantially less diverse than in the Clarkforkian, synchronous over a specified geographic region (29). however (13, 14). It appears that the plant record cannot account ky, a segment of geologic time 1,000 y in duration or the age of an event (e.g., for the dramatic increase in mammal taxa and FADs. Immigra- 200,000 years ago) without reference to a point or a set of points on the tion, then, was of supreme importance in driving faunal inno- radioisotopic time scale. vation in the early Wasatchian, during the PETM. The faunal LAD, the last stratigraphic occurrence of a taxon, considered to have been dynamics of Wa-0 are strongly associated with a positive pulse in synchronous over a specified geographic region (29). climate warming. Ma, Megannum. One million years in the radioisotopic time scale. Diverse floras of tropical to subtropical aspect are recorded at m.y., a segment of geologic time 1 million years in duration or the age of an the beginning of the EECO and these continue, along with event without reference to the radioisotopic time scale. increasing MAT by Wa-7 (Fig. 1 and Table 1). In the absence of NALMA, an interval of time based on mammalian biochronology (30). PETM, a short-term dramatic pulse of global warming at the Paleocene– notable immigration in the EECO, faunas in Wa-6 and Wa-7 Eocene boundary. show a strong increase in genera compared with Wa-5, with a Floral terms follow the vegetation classification of Graham (31). comparable increase in both FADs and LADs (Table 1 and Fig. 2), and this pattern continues into Br-1a, all within the EECO. Mammalian Biochrons. The mammalian biochron time scale follows Secord et The nearly equal diversity of FADs and LADs in Wa-6–Wa-7 al. (2) from Tiffanian Ti-3 to Wasatchian Wa-1 and figure 8.5 from Woodburne and the preponderance of FADs versus LADs in Br-1a is in sharp (30) from Wa-1 to Wa-4. The intervals Wa-4 through the early Uintan follow contrast to the situation in the later part of the EECO (Br-1b– Smith et al. (32). The Bridgerian revision (32) lowers the Wa-7/Br-1a boundary Br-3) where LADs greatly outnumber FADs, and the generic to Ϸ51 Ma relative to that of Woodburne (30). In addition, Br-0 is not used as diversity shows its greatest decline in any part of the time scale the basal biochron of the Bridgerian based on the observation that the considered herein. Gardnerbuttean subage is indistinguishable from those typically designated Floral turnover and climatic change that persisted in Br-1b– as Br-1a (G.F.G. and R.K.S., personal observation). The faunas of Br-0 and Br-1a in the literature are herein combined into a single unit, Br-1a. See refs. 33–35 Br-3 is contemporaneous with the dramatic faunal change of the for paleobotanical data used in Fig. 1. Additional data and background same interval. It therefore appears inescapable to conclude that discussions are found in ref. 36. faunal changes in both parts of the EECO were driven by climate. The Clarkforkian/Wasatchian boundary increase in diversity ACKNOWLEDGMENTS. The greatest possible appreciation is extended to Dr. [figure 4F in Alroy et al. (1)] incorporates both Wa-0 and Wa-1 of Peter Wilf, whose critique of the paleobotanical parts of this report was our Fig. 1 and appears to be a major result of climate change in their especially valuable. Dr. Christine Janis made preprints of mammalian range charts available from The Evolution of Tertiary Mammals of North America, view. The data we summarize indicate that the taxonomic increase Vol 2. Dr. Jim Mead made insightful and useful comments on an early draft of at the PETM is basically due to a major immigration event that this manuscript as did Dr. Amy Chew, who also provided invaluable assistance reflects high-latitude warming. This is congruent with the inter- in applying Wasatchian NALMA biochrons to the floral record and aided with pretation on page 281L of Alroy et al. (1). On the other hand, on final manuscript revisions. Ken Rose made valuable contributions to the manuscript on which the present article is based. Christine Janis and Paul Koch page 317 of ref. 28, Alroy characterized the event as being only contributed valuable suggestions on earlier versions of this manuscript that indirectly influenced by climate in that it produced biogeographic are greatly appreciated. None of the individuals acknowledged here neces- shifts rather than some other, unspecified response. sarily supports the conclusions reached in this report.

1. Alroy J, Koch PL, Zachos JC (2000) Global climate change and North American mammalian 6. Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse evolution. Deep Time, eds Erwin DH, Wing SL. Paleobiology Suppl 26(4):259–288). warming and carbon-cycle dynamics. Nature 451:279–283. 2. Secord R, et al. (2006) Geochronology and mammalian biostratigraphy of middle and 7. Bains S, Norris RD, Corﬁeld RM, Gingerich PD, Koch PL (2003) Marine–terrestrial upper Paleocene continental strata, Bighorn Basin, Wyoming. Am J Sci 306:211–245. linkages at the Paleocene–Eocene boundary. Causes and Consequences of Globally 3. Gingerich PD (2003) Mammalian responses to climate change at the Paleocene–Eocene Warm Climates in the Early Paleogene, eds Wing SL, Gingerich PD, Schmintz B, Thomas boundary: Polecat Bench record in the northern Bighorn Basin, Wyoming. Causes and E (Geol Soc Am Spec Pap 369), pp 1–9. Consequences of Globally Warm Climates in the Early Paleogene, eds Wing SL, 8. Wing SL, et al. (2005) Transient ﬂoral change and rapid global warming at the Gingerich PD, Schmintz B, Thomas E (Geol Soc Am Spec Pap 369), pp 463–478. Paleocene–Eocene boundary. Science 310:993–996. 4. Clyde WC, Gingerich PD (1998) Mammalian community response to the latest Paleo- 9. Miller KG, Fairbanks RG, Mountain GS (1987) Tertiary oxygen isotope synthesis, sea cene thermal maximum: An isotaphonomic study in the northern Bighorn Basin, level history, and continental margin erosion. Paleoceanography 2:1–19. Wyoming. Geology 26:1011–1014. 10. Prentice ML, Matthews RK (1988) Cenozoic ice-volume history: Development of a 5. Koch PL, et al. (2003) Carbon and oxygen isotope records from paleosols spanning the composite oxygen isotope record. Geology 16:963–966. Paleocene–Eocene boundary, Bighorn Basin, Wyoming. Causes and Consequences of 11. Zachos JC, Pagani M, Sloan IC, Thomas E, Billups K (2001) Trends, rhythms, and Globally Warm Climates in the Early Paleogene, eds Wing SL, Gingerich PD, Schmintz aberrations in global climate 65 Ma to present. Science 292:686–693. B, Thomas E (Geol Soc Am Spec Pap 369), pp 49–64.

13402 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0906802106 Woodburne et al. Downloaded by guest on October 1, 2021 12. Wilf P (2000) Late Paleocene–early Eocene climatic changes in south-western Wyo- 24. Foote M (1992) Rarefaction analysis of morphological and taxonomic diversity. Paleo- ming: Paleobotanical analysis. Geol Soc Am Bull 112:292–307. biology 18(1):1–16. 13. Wing SL, Alroy J, Hickey LJ (1995) Plant and mammal diversity in the Paleocene to 25. Stucky RK (1992) Mammalian faunas in North America of Bridgerian to Early Arika- early Eocene of the Bighorn Basin. Palaeogeogr Palaeoclimatol Palaeoecol reean ‘‘Ages’’ (Eocene and Oligocene). Eocene–Oligocene Climatic and Biotic Evolu- 115:117–155. tion, eds Prothero DR, Berggren WA (Princeton Univ Press, Princeton), pp 464–493. 14. Wing SL (1998) Late Paleocene–early Eocene floral and climatic change in the Bighorn 26. Wolfe JA (1978) A paleobotanical interpretation of Tertiary climates in the Northern Basin, Wyoming. Late Paleocene–Early Eocene Biotic and Climatic Events, eds Aubry Hemisphere. Am Sci 66:694–703. M-P, Lucas S, Berggren WA (Columbia Univ Press, New York), pp 371–391. 27. Wolfe JA, Poore RZ (1982) Tertiary marine and nonmarine climatic trends. Effects of Past 15. Smith T, Rose KD, Gingerich PD (2006) Rapid Asia–Europe–North America geographic Global Change on Life, eds Nat Res Council (Natl Acad Press, Washington, DC), pp 154–158. dispersal of earliest Eocene primate Teilhardina during the Paleocene–Eocene Thermal 28. Alroy J (2009) Speciation and extinction in the fossil record of North American mam- Maximum. Proc Natl Acad Sci USA 103(30):11223–11227. mals. Speciation and Diversity, eds Butlin RK, Bridle JR, Schulter KD (Cambridge Univ 16. Hooker JJ (2000) Ecological response of mammals to global warming in the late Press, Cambridge, UK), pp 301–323. Paleocene and early Eocene. GFF 122:77–79. 29. Woodburne MO (1996) Precision and resolution in mammalian chronostratigraphy; 17. Gunnell GF (1998) Mammalian faunal composition and the Paleocene/Eocene Epoch/ principles, practices, examples. J Vertebr Paleontol 16:531–555. Series boundary: Evidence from the northern Bighorn Basin, Wyoming. Late Paleo- 30. Woodburne MO (2004) Global events and the North American mammalian bio- cene–Early Eocene Biotic and Climatic Events, eds Aubry M-P, Lucas S, Berggren WA chronology. Late Cretaceous and Cenozoic Mammals of North America: Biostratig- (Columbia Univ Press, New York), pp 409–427. raphy and Geochronology, ed Woodburne MO (Columbia Univ Press, New York), pp 18. Strait SG (2004) Small, smaller, smallest: A case for dwarfing in small-bodied Wa-0 315–344. mammals. J Vertebr Paleontol Suppl to no. 3, 24:118A. 31. Graham A (1999) Late Cretaceous and Cenozoic History of North American Vegetation 19. Heinrich RE, Strait SG, Houde P (2008) Earliest Eocene Miacidae (Mammalia: Carnivora) (Oxford Univ Press, New York). from northwestern Wyoming. J Paleontol 82:154–162. 32. Smith ME, Carroll AR, Singer BS (2008) Synoptic revision of a major ancient lake system: 20. Tiffney BH (1994) An estimate of the early Tertiary paleoclimate of the southern Arctic. Eocene Green River Formation, western United States. Geol Soc Am Bull 120 (1/2): Cenozoic Plants and Climates of the Arctic, eds Boulter MC, Fisher HC (NATO ASI Series 54–84. 127, Springer, Berlin), pp 267–293. 33. Wing SL, Greenwood DR (1993) Fossil and fossil climate: The case for equable conti- 21. Tiffney BH (2000) Geographic and climatic influences on the Cretaceous and Tertiary nental interiors in the Eocene. Philos Trans R Soc London Ser B 341:243–252. history of Euramerican floral similarity. Acta Univ Carolinea Geol 44:5–16. 34. Wilf P, Wing SL, Greenwood DR, Greenwood CL (1998) Using fossil leaves as paleopre- 22. Beard KC, Krishtalka L, Stucky RK (1992) Revision of the Wind River faunas, early Eocene cipitation indicators: An Eocene example. Geology 26(3):203–206. of central Wyoming, part 12. New species of omomyid primates (Mammalia: Primates: 35. Fricke HC, Wing SL (2004) Oxygen isotope and paleobotanical estimates of tempera- Omomyidae) and omomyid taxonomic composition across the early-middle Eocene ture and *18O-latitude gradients over North America during the early Eocene. Am J Sci boundary. Ann Carnegie Mus 61(1):39–62. 304:612–635. 23. Gunnell GF (1997) Wasatchian–Bridgerian (Eocene) paleoecology of the western in- 36. Woodburne MO, Gunnell GF, Stucky RK (2009) Land mammal faunas of North America: terior of North America; changing paleoenvironments and taxonomic composition of Rise and fall during the Early Eocene Climatic Optimum. Denver Mus Nat Sci Ann omomyid (Tarsiiformes) primates. J Hum Evol 32:105–132. 1:1–80. GEOLOGY EVOLUTION

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