Abrupt perturbations of the global carbon cycle during the early Eocene are associated with rapid global warming events, which are analogous in many ways to present greenhouse warming. Mammal dwarfing has been observed, along with other changes in community structure, during the largest of these ancient global warming events, known as the Paleocene-Eocene Thermal Maximum [PETM; ~56 million years ago (Ma)]. We show that mammalian dwarfing accompanied the subsequent, smaller-magnitude warming event known as Eocene Thermal Maximum 2 [ETM2 (~53 Ma)]. Statistically significant decrease in body size during ETM2 is observed in two of four taxonomic groups analyzed in this study and is most clearly observed in early equids (horses). During ETM2, the best-sampled lineage of equids decreased in size by ~14%, as opposed to ~30% during the PETM. Thus, dwarfing appears to be a common evolutionary response of some mammals during past global warming events, and the extent of dwarfing seems related to the magnitude of the event.

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INTRODUCTION

Climate change affects plants and animals in ways that are poorly understood. Much can be learned from the study of climate change in the geological past and its effect on contemporaneous biotas. Early Eocene global warming events, or “hyperthermals,” are associated with large perturbations of the global carbon cycle and thus serve as analogs of modern-day global warming. The largest of the hyperthermals was the Paleocene-Eocene Thermal Maximum (PETM), which occurred approximately 56 million years ago (Ma) and lasted about 180,000 years (1, 2). The PETM is recognized in the geological record by marine and terrestrial carbon isotope excursions (CIEs) of about −3 per mil (‰) and −3 to −6‰ (2–4), respectively, and an increase in global temperatures of 5° to 8°C within 10,000 years (2, 5, 6).

Consequences of the PETM’s rapid shifts in carbon cycling and atmospheric temperatures were recorded in both marine and terrestrial records, including profound biotic turnover and ecologic change in the terrestrial realm. One of the most extensively studied terrestrial records of the PETM is located in the Bighorn Basin of Wyoming. Here, the event is characterized by transient changes in vegetative composition, from warm temperate paleofloras to those that are indicative of dry tropical and subtropical climates (2). Terrestrial records of the PETM are also accompanied by significant mammalian turnover, including the abrupt introduction of several modern mammalian lineages (including perissodactyls, artiodactyls, and primates) and mammalian dwarfing in both immigrant and endemic taxa, observed through changes in the size of fossilized adult teeth [we use the term “dwarfing” to simply describe an observed size decrease, whether it be an evolutionary response or a response that involves other processes as well (for example, migration and ecophenotypic change)] (7–11). Since the discovery of the PETM in deep-sea cores and continental sections, subsequent smaller-magnitude CIEs have also been discovered in marine records (12, 13). The second largest hyperthermal of the early Eocene, known as ETM2, occurred about 2 million years after the PETM (approximately 53.7 Ma) and was associated with a deep-sea CIE of >1.4‰ and ~3°C warming (12, 13)—about half the magnitude of the PETM (13). Another smaller-amplitude hyperthermal, identified as “H2,” appears in the marine record about 100,000 years after ETM2 (approximately 53.6 Ma), with a CIE of ~0.8‰ and ~2°C warming (13).

More recently, geochemical evidence of ETM2 and H2 was uncovered in terrestrial sedimentary deposits within the Bighorn Basin, with CIEs of −3.8 and −2.8‰, respectively (14, 15). However, their effects on terrestrial climates and ecosystems are not yet documented. Preliminary results indicated that these hyperthermals were not associated with previously identified mammalian turnover events [(14); see the study of Chew (16) for a suggestion of turnover within this interval in the southern Bighorn Basin], and no detailed study has yet been carried out investigating within-lineage mammalian body size change as done for the PETM (17).

Using the newly documented terrestrial records of ETM2 and H2, this study addresses two important questions: (i) Similar to the PETM, is mammalian body size change also found in association with ETM2 and H2? If so, (ii) is there a relationship between the magnitude of a hyperthermal and/or carbon cycle perturbation and the degree of mammalian dwarfing? Understanding the similarities and differences between biotic responses to the PETM and these other smaller hyperthermals is important for determining what kinds of biological responses might be typical for rapid global warming events like what we are experiencing today.

Mammalian fossils used in this study were collected from localities within the northern Bighorn Basin of Wyoming that stratigraphically span known locations of the ETM2 and H2 CIEs. The Bighorn Basin is located in northwestern Wyoming, approximately 130 km east of Yellowstone National Park (Fig. 1). The basin formed during the Laramide orogeny and is bordered by the Beartooth Mountains to the northwest, Bighorn Mountains to the east, and Owl Creek Mountains to the south. It is composed of up to 4500 m of stratigraphically continuous synorogenic continental sedimentary deposits that accumulated through the early Paleogene (18–20). The fossils in this study are from the Willwood Formation, which is composed dominantly of channel sandstones and brightly colored pedogenically modified overbank mudstone deposits (paleosols), suggesting paleoenvironments of open-canopy forests and relatively dry floodplains (21, 22). Aside from numerous fossil mammals, the Willwood Formation also preserves fossil reptiles, birds, amphibians, and plants (18). The early Cenozoic began with minimal-to-no polar ice caps and high global temperatures that reached their long-term peak during the Early Eocene Climatic Optimum (~52 to 50 Ma) (23). Within the Bighorn Basin, atmospheric mean annual temperatures during the PETM were estimated to reach between 19° and 26°C (2, 6, 24).

Fig. 1 Bighorn Basin and sample localities. The Bighorn Basin is located in northwestern Wyoming, USA. Upper Deer Creek (UDC), Gilmore Hill (GH), and White Temple (WT) stratigraphic sections are located within the McCullough Peaks region of the northern Bighorn Basin (outlined by a dashed box, see close-up in fig. S1).

The thick, stratigraphically continuous [on 100,000-year to 400,000-year time scales; (15)] deposits of the Bighorn Basin have long promoted high-resolution studies of ecology, evolutionary trends in flora and fauna, and most recently, past climate (2, 25, 26). Since the early 1990s, stable carbon isotope studies of pedogenic carbonates have been conducted in the paleosols of the basin to develop continental records of hyperthermal CIEs (14, 15, 27–29). The carbon isotopic composition of pedogenic carbonate is useful for recording CIEs because soil CO 2 , from which the carbonate precipitates, ultimately tracks atmospheric δ13C (27). Today, soil CO 2 at depths greater than ~30 cm is dominantly a product of root respiration and within-soil organic matter decomposition because atmospheric CO 2 has an insignificant direct influence at this depth (30, 31). Combining a ~4.4‰ 13C enrichment (relative to plant tissue) through diffusion of CO 2 to the atmosphere with an enrichment of ~10.5‰ due to temperature-dependent carbonate precipitation fractionations, the δ13C of soil carbonates today mirror the δ13C of overlying flora with an offset of ~−15‰ (28, 30, 31). Because pCO 2 may have changed over time, it should be noted that these 13C enrichment values are present-day estimates (32–34). Carbonate nodules will form when high soil CO 2 production and organic decay lead to acidic solutions that leach the upper part of the soil. These fluids percolate down into the soil and, in combination with an increase in the concentration of Ca2+ or pH, promote calcite precipitation (30).

Through the use of carbon isotope analyses of pedogenic carbonate, ETM2 and H2 have recently been identified in the McCullough Peaks region of the northern Bighorn Basin (fig. S1). Five stratigraphic sections now capture the ETM2 and H2 CIEs in this area—GH (Gilmore Hill), WT (White Temple), UDC (Upper Deer Creek), WB (West Branch), and CSH (Creek Star Hill). GH and UDC were first reported by Abels et al. (14), WB and CSH were first reported by Abels et al. (15), and WT is newly described in this study. This study also provides an updated, higher-resolution, GH isotope section that leads to a revised correlation between GH and UDC. Our updated version of the GH isotope section integrates both the new data and the previous data by Abels et al. (14). The stratigraphic sections are correlated via tracing of stratigraphic horizons, including a distinct purple marker bed known as Purple 2 [P2; first identified by Abels et al. (14), which lies in the center of the ETM2 CIE in all sections; Fig. 2 and fig. S2]. The correlation of these sites has also been constrained through magnetostratigraphy and correlation of the CIEs (14, 15). In addition, precession and eccentricity scale patterns from the McCullough Peaks CIEs are very similar to marine CIE patterns, further confirming correlations between sections (15).

Fig. 2 Stratigraphic framework. Lithostratigraphy, paleosol carbonate nodule isotope stratigraphy (δ13C pc ), biozonation, and magnetostratigraphy of the GH, WT, and UDC sections. The tan-shaded region highlights the body of ETM2 across all sections. The purple band represents the P2 marker bed, which can be visually traced across all outcrop sections in the field, and is associated with the most negative values of the ETM2 CIE. *Modified from Abels et al. (14).

Stable isotopes of fossil mammal tooth enamel were analyzed to complement the paleosol carbonate analyses, to confirm the stratigraphic position of specimens within the CIEs, and to investigate the paleoecology of these extinct taxa. Because of the precipitation of mammal tooth enamel during ontogenesis, certain teeth may serve as records of an organism’s paleoecology, including isotopic information about ingested water and consumed vegetation. This is possible because tooth enamel is composed of bioapatite, Ca 5 (PO 4 , CO 3 ) 3 (OH, CO 3 ), which precipitates in equilibrium with body water (35–37). Furthermore, in terms of preservation, enamel is more resistant to recrystallization and postmortem diagenesis than is bone or dentine because of comparatively smaller amounts of collagen and a larger crystal size (38, 39).

Carbon isotopes in tooth enamel of noncarnivores reflect the δ13C of consumed vegetation, which tracks δ13C atmosphere through isotopic fractionation processes associated with photosynthesis (33, 39, 40). Oxygen isotopes in mammalian body water ultimately record the isotopic values of ingested meteoric water and, with the use of established physical models for a range of mammal sizes, can be used to estimate δ18O meteoric water , which is in turn linked to local atmospheric temperature (35–37, 39, 41).

Using tooth size as a proxy for body size, evidence for mammalian dwarfing has been recorded in terrestrial records of the PETM (7, 8, 10). Teeth in adult mammals scale proportionally to body size. Of all tooth positions, the first lower molar (M 1 ) tends to exhibit the strongest correlation between crown area and body weight across most taxonomic groups of mammals. However, the crown area of other molars are also highly correlated with body size (see Materials and Methods for further discussion of body size calculations) (42–44). A high-resolution study focusing on the earliest equid Sifrhippus demonstrated a decrease of at least 30% in body size during the first 130,000 years of the PETM, followed by a 76% rebound in body size during the recovery phase of the PETM. It is possible that the PETM records begin on an unconformity within the central and southern Bighorn Basin, and as a result, early PETM fossil records may not encapsulate the true extent of dwarfism. Assuming pre- and post-PETM environmental conditions were equal, pre- and post-PETM body size could also be assumed as equal. In this case, on the basis of a comparison between mid- and post-PETM body size cited in the high-resolution study of Secord et al. (10), the extent of early equid PETM dwarfing may have reached ~44%.

For the purpose of comparison, our ETM2 and H2 study focuses on body size change in the early equid lineage Arenahippus pernix (see Materials and Methods for note on taxonomy). Fossils of early equids are common in lower Eocene deposits of the Bighorn Basin, making a comparison between the PETM and ETM2 hyperthermal events possible. This study further investigates three other commonly occurring mammalian lineages: Diacodexis metsiacus, an early rabbit-sized artiodactyl that had cursorial/saltatorial locomotive adaptations (45); Hyopsodus simplex, a generalist herbivorous archaic ungulate with weasel-like body proportions (45); and Cantius abditus, an early frugivorous primate similar to modern lemurs (45), although sample sizes for these three lineages were less favorable.