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 temper- ature 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 lin- eages (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 mam- malian 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 tran- sient excursion at the PETM and a similarly warm in- terval 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 di- versity pattern generally reflects the MAT record, ex- cept 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).