Paleobiology, 35(4), 2009, pp. 587–611

Using ecological niche modeling for quantitative biogeographic analysis: a case study of and in the Great Plains

Kaitlin Clare Maguire and Alycia L. Stigall

Abstract.—The subfamily Equinae in the Great Plains region of underwent a dramatic radiation and subsequent decline as climate changed from warm and humid in the middle Miocene to cooler and more arid conditions during the late Miocene. Here we use ecological niche modeling (ENM), specifically the GARP (Genetic Algorithm using Rule-set Prediction) modeling system, to reconstruct the geographic distribution of individual species during two time slices from the middle Miocene through early Pliocene. This method combines known species occurrence points with environmental parameters inferred from sedimentological variables to model each species’ fundamental niche. The geographic range of each species is then predicted to occupy the geographic area within the study region wherever the set of environmental parameters that constrain the fundamental niche occurs. We analyze changes in the predicted distributions of individual species between time slices in relation to Miocene/Pliocene climate change. Specifically, we examine and compare distribution patterns for two time slices that span the period from the mid-Miocene (Barstovian) Climatic Optimum into the early Pliocene () to determine whether habitat fragmentation led to speciation within the clade and whether species survival was related to geographic range size. Patchy geographic distributions were more common in the middle Miocene when speciation rates were high. During the late Miocene, when speciation rates were lower, continuous geographic ranges were more common. Equid species tracked their preferred habitat within the Great Plains region as well as regionally throughout North America. Species with larger predicted ranges preferentially survived the initial cooling event better than species with small geographic ranges. As climate continued to deteriorate in the late Miocene, however, range size became irrelevant to survival, and rates increased for species of all range sizes. This is the first use of ENM and GARP in the continental fossil record. This powerful quantitative biogeographic method offers great promise for studies of other taxa and geologic intervals.

Kaitlin Clare Maguire. Department of Integrative Biology, University of , Berkeley, California 94720. E-mail: [email protected] Alycia L. Stigall. Department of Geological Sciences and OHIO Center for Ecology and Evolutionary Studies, Ohio University, Athens, Ohio 45701. E-mail: [email protected]

Accepted: 9 February 2009

Introduction mosaic of savanna and riparian forests that The subfamily Equinae underwent a major supported browsing, grazing, and mixed- radiation during the Miocene from one feeding (Webb 1983). Following the species, leonensis, to 70 species, radiation, members of the Equinae exhibit a reaching its highest diversity during the variety of dental and muzzle morphologies as middle Miocene (Clarendonian) with 13 well as a diverse range of body sizes and limb named genera (MacFadden 1992; Hulbert proportions (MacFadden 1992). It has been 1993) (Fig. 1). The main interval of equid previously hypothesized that this morpho- radiation coincides with the first major logical diversity arose as equids with over- cooling event of the Miocene (Zachos et al. lapping distributions partitioned their niches 2001), and the equid radiation has been to exploit different resources as climate classically attributed to an adaptive response changed (MacFadden 1992; Webb et al. following climate and vegetation change 1995). This diversity peak, however, did not during the Miocene (MacFadden and Hulbert last. The equid clade began to decline during 1988; Hulbert 1993). As the climate became the late Miocene, and by the middle of the cooler and drier during the Miocene, vegeta- Pliocene only three genera were extant (Hul- tion shifted from woodland dominated to a bert 1988). Competition with other grazers

’ 2009 The Paleontological Society. All rights reserved. 0094-8373/09/3504–0007/$1.00 588 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

FIGURE 1. Temporally calibrated cladogram of Equinae modified from Maguire and Stigall (2008). Time slice divisions are indicated at the top. Narrow horizontal lines indicate ghost lineages, whereas bold horizontal lines indicate the recorded range. Thick gray lines indicate species whose ranges were modeled in this analysis. ECOLOGICAL NICHE MODELING OF EQUINAE 589

(e.g., artiodactyls, rodents) was previously Although the diversification of the Equinae inferred to have caused the decline of the is hypothesized to have resulted from climate clade (Simpson 1953; Webb 1969, 1984; Stan- change and ecological specialization, the ley 1974), but it is now attributed to the interaction between individual species and continuation of cooling temperatures and environmental conditions has not previously more arid climatic conditions (MacFadden been quantitatively analyzed. Here we recon- 1992; Webb et al. 1995). struct the geographic ranges for individual Most paleobiogeographic studies of equids species of Miocene to early Pliocene horses in have focused on large-scale patterns, such as concert with environmental conditions to migration patterns from North America to the assess how changing climate and shifting Old World (e.g., MacFadden 1992). Other habitats affected evolutionary patterns in the paleobiogeographic studies have grouped Equinae. In order to study the distribution of equids with other Miocene mammalian clades horses relative to ecological changes, we use to demonstrate general patterns, such as ecological niche modeling (ENM). A species’ retreat to the Gulf Coast region as the climate ecological, or fundamental, niche is defined as became cooler and more arid in northern areas the set of environmental tolerances and limits of North America during the late Miocene in multidimensional space that defines where (e.g., Webb 1987; Webb et al. 1995). A more a species is potentially able to maintain focused study examining the distribution of populations (Grinnell 1917; Hutchinson individual equid species can provide a frame- 1957). Determining the ecological niche of a work in which to analyze habitat fragmenta- taxon is essential in determining its potential tion, niche partitioning, and speciation. Be- distribution (Peterson 2001) as well as taxon/ cause the radiation is hypothesized to have environment interactions. A species may resulted from climate change, an integrated potentially occupy the entire geographic assessment of the ecology and biogeography is region in which its ecological niche occurs; necessary to fully understand evolutionary although biotic interactions, including com- patterns in the clade. Shotwell (1961) recog- petition and predation may limit a species nized this relationship in his study on the range to a smaller ‘‘realized niche’’ (Lomolino biogeography of horses in the northern Great et al. 2006). Because determination of these Basin, in which he observed changes in species biotic interactions from the fossil record is composition that coincided with vegetation rarely possible, we turn here instead to change. Shotwell concluded that this shift modeling species’ ecological niches. resulted from immigration of equid species Ecological niche modeling is a GIS-based adapted to the new vegetative regime from method in which species’ environmental other regions into the Great Basin. tolerances are modeled on the basis of a set Recent advances in understanding the of environmental conditions at locations phylogenetic relationships provide a more where the species is known to occur. The robust framework for new analyses. Further- species range is then predicted to occupy more, numerous recent studies have investi- areas where the same set of environmental gated the environmental and climatic condi- conditions occurs in the study region. Funda- tions of the Great Plains during the Miocene. mentally, this approach directly utilizes sed- These studies comprise analyses of vegetation imentary data to determine the likely distri- type (e.g., Fox and Koch 2003; Stro¨mberg bution of taxa, thus providing a framework to 2004; Thomasson 2005), paleosol composition examine interactions between abiotic and (e.g., Retallack 1997, 2007), and climate biotic factors that control species distribution proxies including stable oxygen and carbon and how these shift through time. ENM- isotopes of foraminifera from deep-sea cores based range prediction provides a framework (e.g., Woodruff et al. 1981; Zachos et al. 2001) to test hypotheses about similarities/differ- that provide a rich source of environmental ences in evolutionary and/or biogeographic information previously unavailable for equid patterns exhibited as climate and environ- ecological biogeographic analyses. ments shifts through time (Stigall and Lieber- 590 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL man 2006; Stigall 2008). ENM methods were constrain the rise and fall of the Equinae in originally developed for modern taxa, and relation to environmental and climatic high levels of predictive accuracy have been change. We model ecological niches and documented (Peterson and Cohoon 1999; predict geographic ranges in order to study Peterson 2001; Stockwell and Peterson 2002). how species’ distributions shifted through In particular, analyzing niche conservatism time as a result of climatic and vegetative versus niche shifts in ecological time (e.g., changes. Specifically, we test hypotheses that Peterson et al. 2001, 2002; Nunes et al. 2007) habitat fragmentation led to the diversifica- and predicting the extent of species occur- tion of the clade and that distributional rences for conservation purposes (e.g., Peter- patterns and range size affected the survivor- son et al. 1999; Raxworthy et al. 2003) have ship of individual species are tested. been highly productive. The only prior use of ENM methods for the fossil record examined Methods the geographic ranges of Late Geographic and Stratigraphic Intervals brachiopods in the north Appalachian Basin Geographic Extent.—The geographic distri- across the Frasnian/Famennian (Late Devo- butions of equid species were reconstructed nian) boundary (Stigall Rode and Lieberman 2005). Results of that study indicated that the for each of two successive time slices during computer-learning-based algorithms used in the middle Miocene through early Pliocene in ENM have excellent potential to predict fossil the Great Plains region of North America species ranges from sedimentary parameters. (Table 1). The study area incorporated re- This study uses the GARP (Genetic Algorithm gions of the High Plains, as defined by using Rule-set Prediction) modeling system, a Trimble (1980), which comprises northern computer-learning-based analytical ENM , western , western , package (Stockwell and Peters 1999). GARP , eastern Colorado, southeastern has been successfully used with numerous Wyoming, and southern South Dakota modern mammalian studies investigating (Fig. 2). Although equid species also inhabit- ecological and environmental questions (e.g., ed regions of North America outside the Lim et al. 2002; Illoldi-Rangel and Sa´nchez- study area, we focus our analysis on the Cordero 2004) and in studies of marine Great Plains region because there is abundant invertebrates in the fossil record (Stigall Rode published data on both the distribution of and Lieberman 2005). This study represents equid fossil material and the environmental the first application of ENM and GARP to setting of the region during the Miocene and fossil vertebrates. The fossil record of equids Pliocene. To facilitate analysis of environmen- is densely sampled and abundant locality tal data, we divided the study region into grid information provides a robust record of boxes of 1u longitude by 1u latitude (Fig. 2). where each species lived in North America Subdivision of geographic regions at this (MacFadden 1992). This clade, therefore, is an scale is standard procedure for ENM analyses excellent candidate for ENM analysis. Direct of modern organisms (e.g., Stockwell and mapping of species ranges from known Peterson 2002; Wiley et al. 2003; Illoldi-Rangel occurrence points may underestimate a spe- and Sa´nchez-Cordero 2004), and modern cies’ actual geographic range because of the environmental data are typically presented inherent biases of the paleontological record in this format. Environmental parameter data (Kidwell and Flessa 1996; Stigall Rode 2005). were collected for as many 1u grid boxes as More accurate ranges can be constructed by possible from literature sources (Tables 2, 3, 4). using ENM to model species ranges on the Climatic, Temporal, and Stratigraphic Frame- basis of known occurrence points and envi- work.—Data were collected for two time slices ronmental parameters estimated from the (Barstovian–Clarendonian and Hemphillian– sedimentary record (Maguire 2008). Blancan) in order to analyze the distribution In this study, the distribution patterns of of species through the climatic changes of the individual species are examined to better Miocene and Pliocene. Boundaries for each ECOLOGICAL NICHE MODELING OF EQUINAE 591

FIGURE 2. Study area overlain with 1u 3 1u grid boxes illustrating the distribution of environmental data (black circles) and species occurrence data (white triangles) for the Barstovian–Clarendonian (A) and Hemphillian–Blancan (B) time slices. Base map indicates paleoelevation in meters, modified from Markwick (2007). time slice (Table 1, Fig. 1) were based on widely used in the literature (e.g., Barnosky changes in slope or directional reversals of and Kraatz 2007; Berger 2007; Costeur and temperature trends in the Cenozoic climate Legendre 2008; Gamble et al. 2008; Williams curve of Zachos et al. (2001). This climate et al. 2008). curve is a compilation of global deep-sea The first interval examined in this analysis oxygen and carbon isotope records of benthic spans a 5.5 Ma interval from the middle foraminifera from over 40 Deep Sea Drilling Barstovian North American Land Project and Ocean Drilling Program sites Age (NALMA), as temperatures began to culled from the literature (Zachos et al. 2001) drop dramatically following the Mid-Miocene and is the Cenozoic climate curve most Climatic Optimum (ca. 11.5 Ma), through the

TABLE 1. Species included in niche modeling analysis by time slice. Number in parentheses indicates number of spatially distinct species occurrences included in modeling analysis.

Barstovian–Clarendonian Hemphillian–Blancan martini (25) ansae (9) Calippus placidus (24) Astrohippus stockii (7) Calippus regulus (17) occidentale (8) Cormohipparion occidentale (44) interpolatus (12) Cormohipparion quinni (12) Dinohippus leidyanus (8) tehonense (11) simplicidens (19) coloradensis (12) aztecus (8) Merychippus insignis (15) Nannippus lenticularis (18) Merychippus republicanus (18) Nannippus peninsulatus (8) affine (30) Neohipparion eurystyle (27) Neohipparion trampasense (5) Neohipparion leptode (10) mirabilis (11) Pliohippus nobilis (9) Pliohippus pernix (28) gidleyi (5) Protohippus perditus (18) Protohippus supremus (26) gratum (37) Pseudhipparion hessei (10) Pseudhipparion retrusum (24) 592 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

TABLE 2. Environmental variables studied and end of the Clarendonian NALMA. Stable primary references. oxygen isotope data from benthic foraminif- era indicate falling temperatures during this 1. Percent C4 vegetation (stable isotope data based on tooth enamel* or paleosols{) time that fluctuated with an overall drop from Fox and Fisher 2004* 13uC to about 7.5–9.5uC (Cooke et al. 2008). Fox and Koch 2003{ Passey et al. 2002* This interval of global cooling was mediated Wang et al. 1994* by the formation of permanent ice sheets on Clouthier 1994* Antarctica (Woodruff et al. 1981; Zachos et al. 2. Mean annual precipitation (MAP) 2001; Rocchi et al. 2006; Lewis et al. 2007). Damuth et al. 2002 Uplift of the Cordilleran region during the Retallack 2007 Retallack unpublished data Miocene resulted in development of a rain- 3. Mollic epipedon shadow effect, which in concert with the Retallack 1997 cooling temperatures, resulted in increased Retallack unpublished data aridity in the Great Plains during the middle 4. Ecotope Miocene (Zubakov and Borzenkova 1990; Axelrod 1985 Ward and Carter 1999). Mean annual precip- Gabel et al. 1998 itation fluctuated between 1000 mm and MacGinitie 1962 Stro¨mberg 2004 500 mm during this period, with an overall Thomasson 1980, 1983, 1990, 1991, 2005 trend of decreasing precipitation (Retallack Wheeler and Mayden 1977 2007). Streams flowing eastward from the 5. Crocodilian distribution Cordillera deposited sediment on the Great Markwick 2007 Plains forming the Ogallala Group, an east-

TABLE 3. Environmental data for each grid box in the Barstovian–Clarendonian. MAP 5 mean annual precipitation. Values in parentheses indicate number of data points within the grid box. Coding for environmental variables as follows: Mollic epipedon: 1 5 mollic, 2 5 near-mollic, 3 5 non-mollic. Ecotope: 1 5 woodland, 2 5 savanna with surrounding woodland, 3 5 savanna, 4 5 grassland/steppe. Crocodiles: 0 5 absence, 1 5 presence. Decimal values represent averaged values where multiple data points occur in a single grid box.

Long. Lat. % C4 MAP (mm) Mollic epipedon Ecotope Crocodilian presence 2102.5 43.5 - - - 3 (1) - 2101.5 43.5 - 266.17 (1) 3 (1) 3 (11) - 2100.5 43.5 - - - - 0 (1) 299.5 43.5 - 356.31 (17) 2.9 (17) 3 (9) 0 (1) 297.5 42.5 13 (1) - - - 1 (2) 298.5 42.5 16 (3) 1590.65 (1) - 2.5 (2) 1 (1) 299.5 42.5 18.4 (6) 819.07 (4) 2 (3) 3 (7) 0 (3) 2100.5 42.5 10.6 (5) 519.57 (15) 2.1 (13) 3 (12) 1 (1) 2101.5 42.5 15 (1) 825 (1) - 2.8 (4) - 2102.5 42.5 16 (1) - - - 0 (1) 2103.5 42.5 13.5 (3) 410.34 (9) 1 (8) - 1 (2) 2104.5 41.5 - 325.86 (1) - - 0 (1) 2103.5 41.5 18.5 (2) - - - 0 (1) 2102.5 41.5 28 (1) 479.59 (3) 2 (2) 2 (1) - 2101.5 41.5 16 (1) - - - - 298.5 40.5 0 (1) 1888.09 (1) - - 0 (1) 2100.5 40.5 23 (1) - - - - 2103.5 40.5 - 1143.92 (1) - 1 (1) - 2104.5 40.5 - 633.87 (1) - - - 2100.5 39.5 21 (1) 402.61 (2) 2.5 (2) 2 (1) - 299.5 39.5 - 266.53 (1) - - 0 (1) 299.5 37.5 - - - - - 299.5 36.5 17.3 (3) - - - - 2100.5 36.5 18 (1) 825 (1) - - 1 (1) 2101.5 36.5 12 (1) - - - 1 (1) 2100.5 35.5 5 (1) - - - 1 (2) 2100.5 34.5 1 (1) 760 (1) - 3 (1) 0 (1) 2101.5 33.5 29 (2) - - - - ECOLOGICAL NICHE MODELING OF EQUINAE 593

TABLE 4. Environmental data for each grid box in the Hemphillian–Blancan time slice. Refer to Table 3 for explanation.

Long. Lat. % C4 MAP (mm) Mollic epipedon Ecotope Crocodilian presence 298.5 43.5 59 (1) 323.53 (1) - - - 297.5 42.5 55 (1) 661.38 (2) - - 0 (1) 298.5 42.5 15 (1) 486.91 (2) - - - 299.5 42.5 37 (3) 379.16 (5) 1.8 (5) - 0 (1) 2100.5 42.5 0 (1) 393.11 (1) 2 (1) - - 2101.5 42.5 58 (1) - - - - 2103.5 42.5 12 (3) 533.87 (1) - - - 2103.5 41.5 26 (2) 335.94 (6) 2.2 (6) - - 2102.5 41.5 27 (5) 349.42 (23) 2.5 (22) 2.7 (3) - 2101.5 41.5 19 (2) 339.2 (5) 2.3 (4) 2 (1) - 2100.5 41.5 - 275.54 (1) - - - 299.5 41.5 15 (1) - - - - 298.5 41.5 21 (1) - - - - 297.5 41.5 69 (2) - - - - 2100.5 40.5 12 (1) 820.2 (1) - - - 2102.5 40.5 - 520.47 (1) - - - 2101.5 39.5 - 646.52 (1) - 4 (1) - 2100.5 39.5 - 429.28 (17) 1.6 (16) - - 299.5 39.5 - 365.76 (27) 2.3 (27) 2 (2) - 297.5 39.5 - 181.26 (1) - - - 299.5 38.5 - 252.52 (2) 3 (2) - - 2100.5 38.5 - 356.51 (27) 2.9 (27) 2 (1) - 2100.5 37.5 38 (2) 503.01 (42) 2.5 (41) - 0 (5) 299.5 37.5 8 (1) 148.43 (1) - - - 299.5 36.5 4 (1) - - - 0 (2) 2100.5 36.5 9.5 (2) - - 3 (1) 0 (3) 2101.5 36.5 - - - - 1 (1) 2102.5 35.5 - - - - 0 (1) 2101.5 35.5 37 (2) - - - 0 (3) 2100.5 35.5 21 (1) - - - 0 (1) 299.5 34.5 - - - - 0 (1) 2100.5 34.5 0 (1) - - - - 2101.5 34.5 43 (3) - - - 0 (2) 2102.5 34.5 20 (1) - - - 0 (1) 2102.5 33.5 11 (1) - - - - 2101.5 33.5 21.5 (2) - - - 1 (3) 2100.5 33.5 - - - - 0 (1) 299.5 33.5 - - - - 1 (1) ward sloping wedge of coarse fluvial sedi- of the Miocene (Zachos et al. 2001; Cooke et ments that eroded from the Laramie and al. 2008). This cooling was associated with Front Ranges (Condon 2005). The Ogallala increased aridity during the Miocene as mean Group sediments include braided stream, annual precipitation dropped to 250 mm alluvial fan, low-relief alluvial plain, and (Retallack 2007). During the early Pliocene, lacustrine deposits (Goodwin and Diffendal however, mean annual precipitation in- 1987; Scott 1982; Swinehart and Diffendal creased to approximately 1050 mm although 1989; Flanagan and Montagne 1993). temperatures continued to cool reaching The second time slice comprises 6.5 million modern temperatures (Chapin and Kelley years and includes the Hemphillian through 1997; Elias and Mathews 2002). Around the Blancan North American Land Mammal 4 Ma, temperatures rose by 10uC, leading to Ages and spans the Miocene-Pliocene bound- the mid-Pliocene thermal optimum (Elias and ary. Climate fluctuated during this interval, Mathews 2002). Deposition of the Ogallala but an overall cooling trend continued. Group continued during the first half (late During the early Hemphillian, temperatures Miocene portion) of this time slice. Erosion of stabilized at approximately 8uC but then the western mountain ranges slowed during continued to decline, reaching a minimum the Pliocene, and as deposition slowed, an of 4.5uC before rising back to 8uC by the end unconformity formed above the Ogallala 594 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

Group (Condon 2005). Furthermore, the Great particularly species with sympatric ranges Plains region began to slowly uplift (Morrison (e.g., Calippus regulus, C. placidus, and C. 1987). As the region rose, sediments in the martini), it is not possible to model these western Great Plains were eroded and either interactions within a paleobiologic frame- redeposited on top of the Ogallala Group or work or with ENM methods. This analysis, removed completely; however, sediments therefore, focuses on reconstructing a species’ accumulated in Nebraska during the Pliocene fundamental niche and not its realized niche. due to its northeastward slope at the time To model fundamental niches of extinct (Steven et al. 1997). species, environmental factors are estimated from sedimentological variables collected Species Occurrence Data from the sedimentary record (Stigall Rode Species occurrence data were collected and Lieberman 2005). This study focused on from the primary literature as well as online five environmental parameters: percent C4 databases (Miocene Mammal Mapping Proj- vegetation, mean annual precipitation, soil ect [MIOMAP]; Carrasco et al. 2005) and the type, ecotope, and crocodilian occurrence (a Paleobiology Database [PBDB]). Species temperature proxy). Each of these parameters name, geographic occurrence (latitude and can be determined from the sedimentary longitude), and stratigraphic position were record, either through fossils or directly from recorded for each species assigned to the sedimentary deposits. The combination of subfamily Equinae (see Supplementary Ma- these variables produces a robust data set of terial online at http://dx.doi.org/10.1666/ environmental and climatic factors that can be 08048.s1:). Alroy’s (2002, 2007) reidenti- used to reconstruct the distribution of fications of several specimens in the PBDB species. The use of five environmental vari- record were honored. The occurrence data ables is consistent with standard ENM meth- were split into the two times slices described odology; analyses with the GARP modeling above. Although species occurrence data system have been successful with as few as were collected for all species considered four and as many as 19 environmental factors valid in recent phylogenetic hypotheses (e.g., (e.g., Peterson and Cohoon 1999; Anderson et Hulbert 1993; Kelly 1995, 1998; Prado and al. 2002; Feria and Peterson 2002). Although Alberdi 1996; Woodburne 1996) (Fig. 1), covariation among these environmental vari- species with fewer than five spatially ables exists (e.g., ecotope and percent C4 distinct occurrences in the study region per vegetation), GARP is not sensitive to covari- time slice were excluded from the analysis. ation among environmental variables because This cutoff number has been determined from it is a Bayesian-based system that produces modeling experiments to be the minimum accurate results for a wide range of domains, data required to produce robust ecological such as numerical function optimization, niche models using the GARP modeling adaptive control system design, and artificial system (Peterson and Cohoon 1999; Stock- intelligence tasks (Stockwell and Peters 1999). well and Peterson 2002). A recent revision of Classical and parametric statistics, on the Cormohipparion by Woodburne (2007) was not other hand, are sensitive to covariation within included in this study because that revision data and, therefore, are not applicable for this utilized highly typological species concepts study. The five environmental parameters are that differ from all previous analyses. discussed individually below, and data are presented in Tables 3 and 4. Environmental Data Stable Carbon Isotopes.—During the Cenozo- A variety of environmental factors (e.g., ic, the dominant vegetation type shifted from temperature, climate, vegetation, resource enclosed forests with leafy shrubs and trees availability) may determine the ecological (C3 plants) to grasslands (C4 plants). This shift niche of a horse species. Although biotic in vegetation created a mosaic of food sources competition may have played a role in further for equid taxa during the Miocene, promoting constraining the ranges of certain species, a diverse range of morphological feeding ECOLOGICAL NICHE MODELING OF EQUINAE 595 adaptations in the Equinae clade (MacFadden of human fossil fuel burning (Friedli et al. 1992; Webb et al. 1995). The distribution of a 1986). We used the results of Fox and Koch species’ food resource is the primary factor (2003) and Passey et al. (2002) to convert raw determining its ecological niche and geo- stable carbon isotope data into percent C4 graphic range (Fox and Fisher 2004; Lomolino vegetation. Percent C4 vegetation was used as et al. 2006). Carbon isotope composition (d13C) an index of the vegetative composition. Low can be used as a proxy for vegetation type (C3 C4 percentages are interpreted as predomi- or C4) in the Great Plains. C3 and C4 plants nantly leafy vegetation preferred by brows- use different photosynthetic pathways (Cal- ers, high percentages are interpreted as vin cycle and Hatch-Slack cycle, respectively) predominantly grassy vegetation preferred for fixing atmospheric CO2 (Cerling and by grazers, and intermediate percentages Quade 1993). Each pathway fractionates represent vegetation preferred by mixed carbon isotopes to a different degree, produc- feeders. ing nonoverlapping carbon isotope composi- Mean Annual Precipitation.—Rainfall would 13 tions. Modern C3 plants exhibit a d C range have directly influenced the vegetation and of 222% to 235% with an average of 227% water resources available to equid species (O’Leary 1988; Tieszen and Boutton 1989), and thus represents a fundamental parameter whereas modern C4 plants exhibit a range of of a species’ ecological niche (e.g., Anderson 210% to 214% with an average of 213% et al. 2002; Illoldi-Rangel and Sa´nchez-Cor- (O’Leary 1988; Tieszen and Boutton 1989). A dero 2004). Mean annual precipitation (MAP) third pathway, crassulacean acid metabolism values determined from paleosols, ungulate (CAM), results in carbon isotope composi- tooth size, and vegetation were compiled for tions intermediate to the other two pathways, analysis (Table 2). The depth of the Bk but it is primarily utilized by succulent plants horizon in paleosols can be utilized to in arid conditions (Cerling and Quade 1993) estimate MAP with the equation: p 5 137.24 and uncommon in the study area. + 6.45D 2 0.013D2, where D is depth in cm Stable carbon isotope data included in this (Jenny 1941; Retallack 1994, 2005). A second study were assembled from published litera- measure of MAP, which uses ungulate tooth ture sources that analyzed d13C primarily size within a community, is ‘‘per-species from paleosols (Table 2). Stable carbon iso- mean hypsodonty’’ (PMH). Developed by tope data from tooth enamel of equids and Damuth et al. (2002), PMH is the average proboscideans were also used to supplement hypsodonty of the ungulate fauna divided by the larger paleosol data set (Table 2). The use the number of all mammalian species present of stable carbon isotope values from tooth in a community (Janis et al. 2004). Lastly, we enamel has been used as a vegetation proxy used MAP ranges interpreted from plant in previous analyses (e.g., Wang et al. 1994; assemblages (Axelrod 1985; Thomasson 1980). Cerling et al. 1997; Passey et al. 2002). While Mollic Horizon.—Soil horizons can provide we recognize that values from tooth enamel information about precipitation, climate, and may be more indicative of diet type than of vegetation cover. As discussed above, these overall environment in certain taxa, we have factors influence the distribution of species. combined stable carbon isotope data from Modern soils supporting grassy vegetation multiple taxa in order to prevent bias in the have a mollic epipedon, a surface layer data set. Studies of carbon isotopes in consisting of dark organic clayey soil about paleosols applied an enrichment value of 2–5 mm thick (Retallack 1997). In paleosols, +14–17% to all values according to Cerling mollic epipedons are recognized by common et al. (1989, 1991). Enamel studies applied an dark, thin, clayey rinds to abundant small enrichment factor of +14% to all values rounded soil peds and by abundant fine root according to Cerling and Harris (1999). traces. In addition, fossilized mollic epipe- Published d13C values also control for the dons are nutrient-rich and often contain 1.5% decrease in the atmospheric composi- carbonate or easily weathered minerals. Re- tion of CO2 that has occurred since the onset tallack (1997, personal communication 2007) 596 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL divided paleosols containing calcareous nod- their distribution (Woodburne 1959; Martin ules from the Great Plains during the Miocene 1984; Markwick 1996). The data set used in this into three categories. The first category, mollic, analysis is derived from the comprehensive contained all paleosols that adhered to the work of Markwick (1996, 2007). Markwick above criteria. The second category, near- (1996) compiled a global database of vertebrate mollic, was assigned to paleosols that had assemblages and used the distribution of surface horizons with ‘‘a structure of suban- crocodilians as a paleotemperature proxy from gular to rounded peds some 5–10 mm in size, the through the . Mark- along with abundant fine root traces and wick (1996) includes crocodilians that belong to darker color than associated horizons’’ (Retal- the ‘‘crown group’’ (Alligatoridae, Crocodyli- lack 1997). Near-mollic epipedons are found dae, and Gavialidae families). The climatic under bunch grasslands of woodlands or tolerance of the modern American alligator, under desert grasslands (Retallack 1997). The Alligator mississippiensis, was used as the third category, non-mollic, was assigned to all minimum temperature tolerance of extinct other paleosols included in the study. This crocodilians. Alligator mississippiensis can toler- third group consisted primarily of paleosols ate a mean temperature range of 25–35uC. similar to soils of deserts and woodlands Because crocodilians are well documented in (Retallack 1997). We coded the vegetation the fossil record and Markwick (1996, 2007) cover interpreted from the three categories of includes vertebrate sites lacking crocodilians as mollic epipedons as 1, 2, and 3, respectively. a control group, crocodilian absences in his Ecotope.—The fourth environmental vari- database are considered true absences. This able included in this analysis is ecosystem study includes 95 assemblages from Markwick type as determined from paleobotanical stud- (2007) that fall within the study area. For this ies (Table 2). Although an extensive collection study, crocodilian presence and absences were of paleobotanical occurrences and taxonomic coded 1 and 0, respectively. descriptions exists in the literature, only studies that included a paleoenvironmental Creation of Environmental Layers description were included in the data set for this analysis. These environmental descrip- For analysis of environmental data, the tions were coded and divided into four study region was divided into 1u grid boxes categories: using latitude and longitude coordinates, as discussed above, and environmental param- 1. Woodland (e.g., ‘‘deciduous valley and eters derived from the literature were as- riparian forests with scattered grass- signed to the appropriate grid box. When lands’’ [Axelrod 1985]) multiple data points occurred in one grid box, 2. Savanna or subtropical grassland with the values were averaged to account for surrounding wooded areas (e.g., ‘‘sub- environmental variability. This method of tropical grassland with associated mesic intermediate coding has been successful with and woody components’’ [Thomasson ENM analysis and is an effective method of 2005]) representing environmental variability (Sti- 3. Savanna or subtropical grassland (e.g., gall Rode and Lieberman 2005). Raw data are ‘‘grassland savanna’’ [Gabel et al. 1998]) included in the supplementary material. 4. Dominantly grassland/Steppe (e.g., Environmental data points for both time ‘‘grassland, shrubs, with limited trees’’ slices were imported into ArcGIS 9.2 (ESRI [Thomasson 1990]) Inc. 2006). For each environmental variable Crocodilian Distribution.—In the fossil rec- we used four data points to create an ord, crocodilian occurrence has traditionally interpolated surface using inverse distance been used as a paleotemperature proxy (Lyell weighting, a method that allows us to use a 1830; Owen 1850). Ecological analysis of set of scattered points to assign values to modern crocodilians indicates that tempera- unknown points. Each interpolated surface ture is the most influential factor determining had a power of 3 (exponent of distance) and ECOLOGICAL NICHE MODELING OF EQUINAE 597

FIGURE 3. Examples of environmental variable interpolations. A, Interpolation of the percentage of C4 vegetation derived from stable isotope data in the Hemphillian–Blancan time slice. B, Interpolation of crocodilian presence/ absence data for Barstovian–Clarendonian; 0 5 absence, 1 5 presence. See Figure 2 for base map explanation. an output cell size of 0.1u (8 3 11 km). used in previous niche modeling analyses of Interpolation was based on four data points paleontological data (Stigall Rode and Lieber- because this was the largest number of data man 2005) because genetic algorithms are points appropriate for interpolation that were effective for data sets with unequal sampling available from all environmental data sets. The and poorly structured domains (Stockwell interpolated environmental area for the Bar- and Peterson 2002). Other statistical methods stovian–Clarendonian and the Hemphillian– such as multiple regression and logistic Blancan time slices covered from 104uW,44uNto regression, assume multivariate normality 98uW,34uNandfrom104uW,44uNto97uW,33uN, and true absence data. Because absence in respectively. Examples of interpolated environ- paleontological data does not necessarily mentalcoveragesareshowninFigure3. represent true absence and multivariate nor- mality is unlikely with paleontological data, Distribution Modeling these methods are not suitable here. Genetic A genetic algorithm approach was chosen algorithms apply a series of rules in an to model the distribution of Equinae species. iterative, evolving manner to the data set Genetic algorithms have been successfully until maximum significance is reached (Stock- 598 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL well and Peters 1999). GARP was specifically abundant species from the Barstovian–Clar- designed to predict a species’ range from its endonian time slice (Cormohipparion occiden- fundamental niche as estimated from envi- tale, Neohipparion affine, Pliohippus pernix, ronmental variables (Peterson and Vieglais Protohippus supremus, Pseudhipparion gratum) 2001). Another advantage of the GARP were used in the jackknifing procedure. The modeling system is that it was originally contribution of each environmental variable designed to accommodate for data from to model error, measured by omission and museum collections; in particular, GARP is commission, was analyzed using a multiple able to analyze non-uniformly distributed, linear regression analysis in Minitab 14 sparse, or patchy data (Peterson and Cohoon (Minitab Inc. 2003). An environmental vari- 1999; Stockwell and Peters 1999). Further- able was inferred to increase error in the more, covariance between environmental var- model if it was significantly correlated with iables does not negatively affect the model’s either omission or commission. A multiple results (Stockwell and Peters 1999). linear regression analysis was conducted for All species distribution modeling was the five species in the Barstovian–Clarendo- performed using DesktopGARP 1.1.4 (www. nian time slice together as well as each nhm.ku.edu/desktopgarp). GARP is com- individual species in the Barstovian–Claren- posed of eight programs that include data donian time slice. Although each environ- preparation, model development, model mental variable is significantly correlated application, and model communication with error with at least one species; no (Stockwell and Peters 1999). The GARP environmental variable contributed signifi- system divides the data in half to create two cant error in all species. All variables were groups, the test group and the training group. therefore considered valid as environmental A rule (e.g., logit, envelope) is randomly predictors and were included in the niche selected and applied to the training set. The modeling analysis. accuracy of the rule is assessed by using Niche modeling was performed individu- 1250 points from the test data set and ally for each species in each time slice. All 1250 points randomly resampled from the rules and all environmental layers to be used area as a whole. The rule is then modified were selected, and 500 replicate models were (mutated) and tested again. If accuracy run for each species with the convergence increases, the modified rule is incorporated interval set at 0.01. Training points were set to into the model; if not, it is excluded. GARP 50% as discussed above. The best subset creates separate rule sets for each region selection was utilized so that the ten best within the study area, rather than forcing a models were chosen, with an omission thresh- global rule across the data. The resulting old of 10% and a commission threshold of 50%. models are more accurate and precise than Range predictions were output as ASCII grids those using global rule methods (Stockwell and the ten best models were imported into and Peters 1999; Stockwell and Peterson ArcGIS 9.2. The ASCII grids were converted 2002). The algorithm continues until further into raster files and weight-summed to derive modification of the rules no longer results in the final range prediction maps (Fig. 4). The improved accuracy or the maximum number geographic area occupied by each species was of iterations set by the operator is reached quantified for biogeographic analysis by using (Stockwell and Noble 1992; Stockwell and the Zonal Geometry Tool in the Spatial Analyst Peters 1999). Toolbox of ArcGIS and then converting the Prior to performing the modeling analysis, number of rasters occupied into percent area the statistical significance of each environ- occupied in km2 (Table 5). mental variable was tested using a jackknifing procedure. This was accomplished by select- Examination of Distributional Patterns and ing all combinations of rules and selected Habitat Tracking layers for the GARP analysis following Stigall Habitat Fragmentation.—We analyzed the Rode and Lieberman (2005). The five most relative prevalence of patchy ranges, ranges ECOLOGICAL NICHE MODELING OF EQUINAE 599

FIGURE 4. GARP predicted species distribution maps for Pseudhipparion gratum in the Barstovian–Clarendonian time slice (A), Nannippus lenticularis in the Hemphillian–Blancan time slice (B), N. azetecus in the Hemphillian–Blancan time slice (C), Astrohippus ansae in the Hemphillian–Blancan time slice (D), Dinohippus interpolatus in the Hemphillian– Blancan time slice (E), Pliohippus mirabilis in the Barstovian–Clarendonian time slice (F), P. pernix in the Barstovian– Clarendonian time slice (G), and P. nobilis in the Hemphillian–Blancan time slice (H). Color ramp indicates number of the ten best models predicting species occurrence. 600 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

TABLE 5. Geographic ranges predicted for species in the Barstovian–Clarendonian and Hemphillian–Blancan time slices from GARP modeling. Explanation of column headings and abbreviations: Area (km2), total area of predicted species range. Coverage, percentage of the study region that is occupied by the predicted species range. Survivor, species survival. S, species survived the NALMA boundary. E, species went extinct by the NALMA boundary. Southern coverage, percentage of area below 39uN (Hemphillian–Blancan time slice) or 38.5uN (Barstovian– Clarendonian time slice) in the study region that is occupied by the predicted species range. No. of populations, the number of distinct populations within a predicted species range. NALMA boundary abbreviations: Bar, Barstovian; Clar, Clarendonian; Hemph, Hemphillian; Bla, Blancan.

Area Coverage Survivor Survivor Southern No. of Species (km2) (%) Bar/Clar Clar/Hemph coverage (%) populations Time slice Cormohipparion occidentale 2.29 3 105 37.45 S S 36.97 2 Bar–Clar Calippus martini 2.32 3 105 37.88 S E 44.83 2 Bar–Clar Calippus placidus 2.64 3 105 43.07 S E 50.07 3 Bar–Clar Calippus regulus 9.15 3 104 14.93 S E 7.13 4 Bar–Clar Cormohipparion quinni 6.45 3 104 10.53 E - 0.17 2 Bar–Clar Hipparion tehonense 1.17 3 105 27.93 S S 36.93 3 Bar–Clar Merychippus coloradensis 6.76 3 104 11.03 E - 0.00 3 Bar–Clar Merychippus insignis 1.10 3 105 17.95 E - 1.33 3 Bar–Clar Merychippus republicanus 8.40 3 104 12.70 E - 0.00 2 Bar–Clar Neohipparion affine 1.67 3 105 27.25 S E 12.93 3 Bar–Clar Neohipparion trampasense 9.34 3 104 15.25 S S 19.20 2 Bar–Clar Pliohippus mirabilis 1.49 3 105 24.28 E - 3.57 2 Bar–Clar Pliohippus pernix 2.66 3 105 43.35 S E 54.20 2 Bar–Clar Protohippus perditus 1.52 3 105 24.76 E - 6.10 2 Bar–Clar Protohippus supremus 1.31 3 105 21.30 S E 14.43 2 Bar–Clar Pseudhipparion gratum 2.23 3 105 36.42 - E 37.23 2 Bar–Clar Pseudhipparion hessei 2.05 3 105 33.40 - E 49.10 1 Bar–Clar Pseudhipparion retrusum 6.83 3 104 11.13 E - 0.00 3 Bar–Clar Astrohippus ansae 2.35 3 105 29.33 - S 31.27 1 Hemph–Bla Astrohippus stockii 2.11 3 105 26.40 - S 46.83 1 Hemph–Bla Cormohipparion occidentale 2.58 3 105 32.21 - S 36.47 1 Hemph–Bla Dinohippus interpolatus 2.65 3 105 33.13 - S 33.79 1 Hemph–Bla Dinohippus leidyanus 3.11 3 105 38.87 - S 22.52 1 Hemph–Bla Equus simplicidens 2.82 3 105 35.30 - - 52.00 3 Hemph–Bla Nannippus aztecus 1.19 3 105 23.87 - - 39.25 1 Hemph–Bla Nannippus lenticularis 4.34 3 105 54.13 - - 33.04 1 Hemph–Bla Nannippus peninsulatus 2.00 3 105 24.96 - - 39.25 1 Hemph–Bla Neohipparion eurystyle 4.29 3 105 53.53 - - 30.42 2 Hemph–Bla Neohipparion leptode 3.67 3 105 45.80 - - 36.62 2 Hemph–Bla Pliohippus nobilis 2.24 3 105 28.00 - S 33.45 1 Hemph–Bla Protohippus gidleyi 2.64 3 105 32.91 - S 29.12 1 Hemph–Bla in which a species’ distribution includes population or patch was defined by a multiple discrete areas of occurrence, versus contained area that did not have a geographic widespread continuous ranges. Habitat frag- connection with a second population. The mentation has been hypothesized to contrib- number of populations per species for each ute to the radiation of numerous clades (e.g., time slice was statistically analyzed using a birds [Mayr 1942]; fishes [Wiley and Mayden two-sample t-test (Table 6). 1985]; [Vrba 1992]). If geographic Range Shift and Habitat Tracking.—Initial patchiness did promote speciation in equids, examination of range models indicated an species should exhibit a higher frequency of apparent southward shift of species between discrete patches in their predicted ranges the time slices, which we analyzed statistical- during the Barstovian–Clarendonian time ly. The study area for each species was slice when speciation rates were higher divided in half along the 39uN latitudinal in (Hulbert 1993), than species in the Hemphil- the Barstovian–Clarendonian time slice time lian–Blancan time slice, when the clade was in slice and the 38.5uN latitudinal in the Hem- decline. For each species in each time slice, we phillian–Blancan time slice. For both time counted the number of discrete populations slices, the percent area occupied by each or patches occupied (Table 5). The extent of a species was calculated using ArcGIS (Ta- ECOLOGICAL NICHE MODELING OF EQUINAE 601

TABLE 6. Two-sample t-test comparing number of discrete populations per time slice.

Source Sample size (n) Mean Standard deviation SE mean Barstovian–Clarendonian 18 2.389 0.698 0.16 Hemphillian–Blancan 13 1.308 0.630 0.17 t statistic 524.50. p 5 1.154 3 1024. d.f. 5 24. ble 5). A two-sample t-test was applied to between species longevity and predicted determine whether species in the Hemphil- distribution area occurs was also assessed lian–Blancan time slice occupied a statistically through regression analysis (Table 8). Specif- larger portion of the southern region of the ically, we tested the hypothesis that species Great Plains than species of the Barstovian– with larger range sizes live longer. The Clarendonian time slice, indicating a range longevity of each species was determined shift to the south (Table 7). from the literature as illustrated in the Only one species, Cormohipparion occidentale, stratocladogram in Figure 1. We also exam- was extant in both time slices. To determine ined the relationship between species survival whether the shifting distribution of C. occiden- across NALMA divisions and the geographic tale from one time slice to another was a extent of a species’ distributional range. function of habitat tracking, the niche model Statistical analyses were performed for each for the Barstovian–Clarendonian time slice Land Mammal Age division within the was projected onto the Hemphillian–Blancan temporal extent of this study (Barstovian/ time slice environmental layers (Peterson et al. Clarendonian, Clarendonian/Hemphillian, and 2001) (Fig. 5). If the resulting distributional Hemphillian/Blancan boundaries). Survival pattern matches the original predicted distri- across the boundary was compared with the bution of C. occidentale for the Hemphillian– size of the species’ predicted range. The area Blancan time slice, then C. occidentale tracked of each species range was determined within its preferred habitat from the Barstovian– ArcGIS by calculating the sum of the areas in Clarendonian time slice to the Hemphillian– which seven or more of the ten best models Blancan time slice (i.e., niche conservatism). If predict occurrence (Table 5). Previous meth- the distributional patterns do not have a high ods have summed three of the five best (Lim degree of overlap, C. occidentale did not occupy et al. 2002), six of the ten best (e.g., Stigall the same niche in both time slices, and the Rode and Lieberman 2005), or all of the ten species would be interpreted to have altered its best (Peterson et al. 2002; Nunes et al. 2007), fundamental niche through time (i.e., niche so our approach is more conservative. Raw evolution). To determine whether the distri- area counts were converted into percentage of butions were equivalent, the area of overlap total model areas for the time slice because the and areal extent not shared were measured in extent of the niche modeling area differs ArcGIS and compared as a percentage of the slightly between time slices (Table 5). A total study area. nonparametric statistical method, Kruskal- Examination of Species Survival versus Wallis, was used to analyze the relationship Range Size.—Whether a general relationship between survival and area because the data

TABLE 7. Two-sample t-test comparing the area of a species’ geographic range in the Southern Great Plains per time slice.

Source Sample size (n) Mean Standard deviation SE mean Barstovian–Clarendonian 18 20.80 20.40 4.8 Hemphillian–Blancan 13 35.69 7.62 2.1 t statistic 522.84. p 5 0.009. d.f. 5 23. 602 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

FIGURE 5. GARP predicted distribution maps. A, Cormohipparion occidentale Barstovian–Clarendonian model projected onto the Barstovian–Clarendonian environmental layers. B, C. occidentale range when the Barstovian–Clarendonian model is projected onto the Hemphillian–Blancan environmental layers. C, C. occidentale Hemphillian–Blancan model projected onto the Hemphillian–Blancan environmental layers. D, C. occidentale range when the Hemphillian–Blancan model is projected onto the Barstovian–Clarendonian environment. are not normally distributed even after log, Fig. 4). All modeled ranges are included in square root, and arcsine transformations were the online Supplementary Material. applied (Tables 9, 10). Habitat Fragmentation Results and Discussion During the Barstovian–Clarendonian time Geographic ranges were modeled for 18 slice, species ranges were divided into more equid species from the Barstovian–Clarendo- discrete populations or patches than during nian time slice and 13 species from the the Hemphillian–Blancan time slice (two- Hemphillian–Blancan time slice (Table 1, sample t-test, p 5 1.15 3 1024) (Table 6, cf. ECOLOGICAL NICHE MODELING OF EQUINAE 603

TABLE 8. Linear regression analysis of species longevity TABLE 10. Kruskal-Wallis test comparing the area of versus the area of a species’ geographic range. species’ geographic range versus species survival across the Clarendonian/Hemphillian boundary. Predictor Coefficient SE coefficient tp Sample size Average Constant 2.84 0.81 3.51 0.001 Source (n) Median rank Z Value Area 0.01 0.03 0.43 0.670 Longevity 5 2.84 + 0.01(Area). Survive 9 33.40 10.0 0.40 SD 5 1.66. Extinct 9 32.21 9.0 20.40 R2 5 0.6. H 5 0.16. p 5 0.691. d.f. 5 1. Fig. 4A,F vs. 4B,E). The relative abundance of patchy habitats in the Barstovian–Clarendo- study area. Chapin and Kelley (1997) reported nian time slice correlates with the mid- increased precipitation in the Pliocene based Miocene interval of rapid cooling. Rapid on the establishment of drainage systems, the cooling has been shown to promote local erosion of Mesozoic and Cenozoic sediments, response of the plant communities resulting the opening of previously closed basins, and in fragmentation of the previously wide- stable isotope compositions of paleosol car- spread woodlands into isolated patches (Vrba bonates in arid lands. Modeled species ranges 1992). Speciation was high during the Bar- for the Hemphillian–Blancan time slice pre- stovian–Clarendonian time slice and the dict species occurrence in the central area Equinae reached its highest diversity at this resulting in more continuous ranges from the time (MacFadden 1992; Hulbert 1993). Frag- northern to southern part of the study area mentation of habitats would necessarily have (Fig. 4B). resulted in patchy species distributions. This Increased continuity of species ranges of in turn would have promoted niche parti- the Hemphillian–Blancan time slice may tioning and speciation via vicariance, giving result partly from the spreading of grasslands rise to the diverse group of mixed feeders, ca. 6–7 Ma into wetter climatic regions (Re- browsers, and grazers that inhabited the tallack 1997). As grasslands spread through- mosaic of vegetation in the Great Plains out the Great Plains in the late Miocene and (Webb et al. 1995). Pliocene, habitats became more homogeneous Environmental coverages of the Barsto- (Axelrod 1985; Webb et al. 1995). The avail- vian–Clarendonian time slice indicate an area able range for species adapted to open of low precipitation, high percentage of C4 grassland and steppe habitats increased, plants, and an absence of crocodilians that promoting large continuous geographic dis- spans the central part of the Great Plains tributions. Continuous ranges resulting from (Fig. 3B). In several predicted ranges for the lack of geographic barriers between popula- Barstovian–Clarendonian time slice, this area tions may have contributed to the reduced is unoccupied (e.g., Fig. 4A). The environ- speciation rates observed within the clade mental coverages for the Hemphillian–Blan- (Hulbert 1993) by eliminating opportunities can time slice indicate a return to wetter for geographic isolation by vicariance, a conditions in this area and a more uniform pattern previously observed in Late Devonian environmental distribution throughout the marine taxa (Stigall 2009). Whereas the diversification of the Equinae

TABLE 9. Kruskal-Wallis test comparing the area of has been attributed to habitat fragmentation species’ geographic range versus species survival across and niche partitioning (MacFadden 1992), its the Barstovian/Clarendonian boundary. decline has been attributed to the inability of Sample Average species to adapt to climatic deteriorations Source size (n) Median rank Z value during the late Miocene and Pliocene (Webb Survive 9 27.93 11.1 2.49 1983; MacFadden 1992). In Hulbert’s (1993) Extinct 7 13.70 5.1 22.49 analysis of biodiversity overturn in Miocene H 5 6.19. to Pliocene Equinae, the observed high p 5 0.013. d.f. 5 1. extinction rates in the late Miocene were 604 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL coupled with low speciation rates that even- points (Fig. 2). The early time slice has a tually decline to zero. Although climatic higher concentration of species occurrence deterioration, as hypothesized by MacFadden points in the northern part of the Great Plains, (1992), may explain the increased rate of whereas the late time slice has a more even extinction, the increase in continuous habitat distribution of points across the Great Plains. following the spread of grasslands, and the Because the GARP algorithm is designed to concomitant reduction in opportunities for analyze data from poorly structured domains speciation, likely contributed significantly to including unevenly distributed species occur- the observed reduction in speciation. Maguire rence data (Stockwell and Peterson 2002), the and Stigall (2008) previously noted that uneven data distribution is unlikely to skew speciation by vicariance occurred much less the resulting range predictions significantly. frequently in equids than in modern conti- Furthermore, the distribution of occurrence nental taxa (e.g., Wiley and Mayden 1985). points in the early time slice may in fact be an Consequently, this additional reduction in the accurate representation of the distribution of amount of vicariant speciation in the Equinae Equinae species, and thus the more northern due to geographic continuity during the late range of equids relative to the late time slice. Miocene and early Pliocene may have been By the Hemphillian, the southwestern influential in the decline of the clade. region of North America was semiarid and dominated by shrubland vegetation (Axelrod Habitat Tracking 1985). Many ungulates retreated from this As temperatures decreased during the region into the Great Plains (Webb et al. 1995). Miocene and the climate became more arid, This included five species that were modeled several species adapted to woodlands and in the Hemphillian–Blancan time slice: Dino- savannas rather than open grasslands retreat- hippus leidyanus, Dinohippus interpolatus, Equus ed to warmer and wetter regions of North simplicidens, Astrohippus ansae, and Astrohippus America, specifically the southern Great stockii (Maguire and Stigall 2008). Maguire Plains and Gulf Coast regions (e.g., Nannippus and Stigall (2008) determined that speciation aztecus, Fig. 4C) (Webb et al. 1995). Using data of these five taxa was a result of geodispersal from carbonate nodules, Retallack (2007) across the Rocky Mountains from the South- identified a climatic gradient from warm west to the Great Plains. Predicted geographic and humid in the coastal regions to cool and distributions of these five species are similar arid in the northern Great Plains region. and occur predominantly on the western edge Species of Equinae in the Hemphillian–Blan- of the Great Plains region (Fig. 4D,E). During can time slice of this study occupied larger the Neogene, the uplift of the Rocky Moun- ranges south of 38.5uN, than species of the tains was interrupted by intervals of tectonic Barstovian–Clarendonian time slice below quiescence (Condon 2005). Consequently, 39uN (two-sample t-test, p 5 0.009) (Table 7). during these intervals of quiescence and This southward biogeographic shift indicates erosion, equid species could migrate across that species tracked their preferred habitat the Cordilleran region, whereas orogenic toward the south as climate changed more pulses resulted in barriers to species move- drastically in the northern regions of North ment. The distribution patterns predicted America. This demonstrates the potential use from niche modeling supports the conclusion of ENM and the fossil record as tools to track of Maguire and Stigall (2008) that speciation patterns of climate change and biogeograph- of these five species was a result of a cyclical ical responses. Further examination of mor- geodispersal process as habitat tracking oc- phological differences and dietary adapta- curred across the Rocky Mountains during tions between species that migrated south these tectonic cycles. and those that retained a northern range As mentioned previously, one species, would further test this hypothesis. The Cormohipparion occidentale, was extant during southward range shift may partially result both time slices. The species’ predicted from the distribution of species occurrence distributions for the Barstovian–Clarendonian ECOLOGICAL NICHE MODELING OF EQUINAE 605 and Hemphillian–Blancan time slices are species’ niche does not occupy the central illustrated in Figure 5A and 5C, respectively. region of the study area (Fig. 5A). In the Any ecological niche model, for example the Hemphillian–Blancan time slice, however, the Barstovian–Clarendonian time slice model, is predicted range does cover this central area, based on the relationship between a species indicating that C. occidentale spread through and its inferred habitat. Once the ecological this region as it tracked its habitat (Fig. 5D). niche of a species is quantified through Unlike other genera of Equinae, Cormohippar- GARP, it is possible to project the model of ion migrated to the Old World during the species occurrence onto either the set of Miocene (Skinner and MacFadden 1977; Mac- environmental variables for the same time Fadden 1992) possibly along with the genus slice (which was conducted for all taxa in the Hipparion (but see Bernor and Armour-Chelu data set) or a different time slice. To test for 1999). Cormohippairon was also one of the last patterns of habitat tracking, the ecological genera remaining in North America at the niche model of C. occidentale developed from end of the Miocene (C. emsliei survived in the the Barstovian–Clarendonian time slice was coastal regions through the Blancan). The projected onto the environmental layers of combination of its longevity and large range both the Barstovian–Clarendonian and Hem- may be a result of its ability to track its phillian–Blancan time slices, as illustrated in preferred habitat when climate shifted. Figure 5A and 5B, respectively. Similarly, the ecological niche model developed from the Range Size versus Survival Hemphillian–Blancan time slice environmen- A positive relationship between geographic tal data for C. occidentale was projected onto range size and species longevity has been both the Barstovian–Clarendonian and Hem- documented in many clades (Stanley 1979; phillian–Blancan time slices, as illustrated in Vrba 1987; Rode and Lieberman 2004; Hen- Figure 5C and 5D, respectively. The percent- dricks et al. 2008). This relationship has not age of overlap of the original projection and been quantitatively assessed in prior analyses the new prediction in the second time slice of equid biogeography; however, this rela- indicates the extent to which the relationship tionship can be analyzed statistically with the between the species and its preferred habitat niche models constructed in this study. No held constant between both time slices. The significant relationship between predicted consistency of this relationship can be re- range size and longevity was recovered when ferred to as habitat tracking. all species ranges modeled from both time Projection of the GARP model for the slices were combined in a single regression Barstovian–Clarendonian time slice onto the analysis (p 5 0.670; Table 8). However, when environmental layers of the Hemphillian– the size of a species’ geographic range was Blancan time slice produced a distribution compared with survival or extinction across that covered 49% of the area originally specific boundaries between NALMA divi- predicted for the Hemphillian–Blancan time sions, a significant relationship emerged. The slice (Fig. 5B,C). This percentage of overlap NALMA divisions (Alroy 2003) are based on suggests that Cormohipparion occidentale first and last appearance data of all mammals tracked its preferred habitat from the Barsto- in North America and are neither dependent vian–Clarendonian time slice into the Hem- on ‘‘immigrant first appearance datum’’ nor phillian–Blancan time slice. In addition, pro- heavily dependent on geochronology data. jection of the Hemphillian–Blancan time slice Species living in the Barstovian that survived GARP model onto the Barstovian–Clarendo- into the Clarendonian had statistically larger nian time slice environmental layers pro- ranges than species that became extinct by the duced a distribution that was 52% similar to end of the Barstovian (Kruskal-Wallis test, p the original distribution for the Barstovian– 5 0.013; Table 9). Clarendonian species that Clarendonian time slice (Fig. 5A,D). The survived into the Hemphillian did not have predicted distribution maps show that during significantly larger ranges than species that the Barstovian–Clarendonian time slice, the became extinct (Kruskal-Wallis test, p 5 0.691; 606 KAITLIN C. MAGUIRE AND ALYCIA L. STIGALL

Table 10). Because only one species of Equi- Pliohippus mirabilis occupied a patchy dis- nae modeled in this study had a stratigraphic tribution in the Great Plains during the range through the Miocene/Pliocene bound- Barstovian–Clarendonian time slice (Fig. 4F) ary, analysis of range size and survival from that covered 24.3% of the study area. Pliohip- the Hemphillian to the Blancan was not pus pernix has been hypothesized to have possible. evolved from P. mirabilis via anagenetic The relationship between survival from one speciation (Hulbert 1993). The patchy pattern NALMA to another and species range size is of P. mirabilis supports the interpretation that likely related to changes in climate and vicariance following habitat fragmentation vegetation during these intervals. During the could have led to the speciation of P. pernix Barstovian, temperatures dropped quickly from an isolated population of P. mirabilis. from 13uC to 7.5–9.5uC (Zachos et al. 2001; During the Barstovian–Clarendonian time Cooke et al. 2008). During this interval of slice, Pliohippus pernix occupied a continuous climate change, vegetation cover was shifting range throughout the Great Plains that cov- and patchy. Under those conditions, the range ered 43.4% of the study area (Fig. 4G). This size of individual species was related to range is larger and more continuous than survival into the Clarendonian. Range size is other ranges modeled for middle Miocene a function of ecological tolerance; consequent- equid species and suggests that P. pernix may ly species with larger ranges were potentially have been an ecological generalist. In fact, P. more broadly adapted and better able to pernix dispersed into the Gulf Coast in the persist through the changing environmental Barstovian–Clarendonian time slice, which conditions. The rapidly changing conditions, further supports a generalist interpretation however, likely were too severe for those with (Maguire and Stigall 2008). The populations of P. pernix that remained in the Great Plains smaller ranges and more restricted ecological are hypothesized to have evolved anageneti- tolerances to survive. During the late Mio- cally into P. nobilis (Hulbert 1993). Pliohippus cene, however, species range size was irrele- nobilis occupied a patchy predicted distribu- vant to survival. Temperatures continued to tion in the Great Plains that covered 28% of drop to approximately 2.3uC during the the total area (Fig. 4H). Although P. nobilis Clarendonian and Hemphillian, accompanied occupied a predominantly southern distribu- by decreasing MAP that reached 500 mm tion in the Great Plains, this species remained (Zachos et al. 2001; Retallack 2007; Cooke et in the Great Plains during the late Miocene al. 2008). Climatic deterioration became too and did not disperse to other regions of North severe even for those species with large America. The patchy geographic range of P. ranges and broad ecological tolerances to nobilis indicates the limited extent of suitable survive. habitat for the species in the Great Plains, Regional Trends potentially an ecological specialist. This eco- logical restriction may have prevented P. Although the Great Plains is analyzed as a nobilis from migrating to other regions of case study for niche modeling because of its North America, for example the Gulf Coast, wealth of available data, equid species also and resulted in its extinction when its inhabited other regions of North America preferred habitat disappeared in the Great during the Miocene. Dispersal between the Plains during the early Hemphillian (Fig. 1). Great Plains and other regions was frequent, The combination of regional and local and the resulting distribution patterns influ- distribution patterns provides a more com- enced speciation patterns within the clade plete picture of the biogeography and evolu- (Maguire and Stigall 2008). One particular tion of Equinae during the Miocene than genus, Pliohippus, clearly demonstrates the either does alone. Here, Pliohippus provides relationship between regional patterns and an example of how the local distribution local (ecological) patterns in the Great Plains pattern is consistent with the regional pattern. region. These five species that migrated into the ECOLOGICAL NICHE MODELING OF EQUINAE 607

Great Plains from the southwest are another during the middle Miocene. Continuous example of how the local pattern supports the ranges may have led to a decrease in regional pattern. Their predicted western speciation rate of the clade due to lack of distribution pattern in the Great Plains sug- subpopulation isolation. Low speciation rate gests (Fig. 4D,E) that they or their ancestors coupled with increased extinction rate from dispersed from the southwestern region of the deteriorating climate resulted in the North America, which is consistent with decline of Equinae in North America. While interpretations based on phylogenetic biogeo- hipparion genera such as Cormohipparion and graphic analyses (Maguire and Stigall 2008). Pseudhipparion became extinct in the Great Plains, species of these two genera did Conclusions survive in the coastal regions of North The geographic ranges of middle Miocene America until the Blancan and Irvingtonian, equid species comprised a higher number of respectively. The genus Equus, however, did discrete populations than late Miocene–early survive into the early Pliocene on the Great Pliocene species. Diversification of the Equi- Plains and was represented by one dominant nae occurred just prior to the middle Mio- species, Equus simplicidens. Further diversifi- cene, indicating that high rates of speciation cation of Equus began only after the hipparion coincided with the distribution of patchy lineages became extinct later in the Pliocene habitats. Habitat fragmentation resulted from (ca. 2 Ma) (MacFadden 1992). changes in vegetation within the Great Plains Finally, niche modeling of horse species in as the climate cooled and became more arid. this study has produced a quantitative, Following dramatic cooling in the Barstovian, detailed framework in which to analyze species with larger ranges survived into the further hypotheses about the relationship Clarendonian better than species with smaller between morphology, ecology, and evolution. geographic distributions. During the late Niche modeling of species ranges in addi- Miocene, however, when temperatures were tional regions, such as the Gulf Coast, would even cooler and the climate more arid, species provide further insight into the final decline range size was irrelevant to survival. The of the clade. In addition, correlating morpho- dichotomy between these intervals may re- logical characteristics of individual species flect differential response of species to rate of with the environmental parameters of their climatic deterioration (rapid versus gradual) predicted niches would provide more de- or that a climatic threshold had been passed tailed information about niche partitioning during the Clarendonian that affected ecolog- and habitat tracking during the Miocene. For ical specialists and generalists equally. Some example, examining the muzzle morphology species, such as Cormohipparion occidentale, of species in this study that showed signifi- exhibited niche conservatism (habitat track- cant migration southward versus those that ing) within the Great Plains as the climate did not may demonstrate whether all species deteriorated. Other species, such as Dinohip- migrated south or only those not specialized pus interpolatus and Astrohippus ansae, tracked in open grassland grazing. their preferred habitats from the southwest- This study is the first quantitative analysis ern region of North America to the Great of ecological biogeography using ENM in a Plains, while others, such as Pliohippus pernix, vertebrate fossil clade. The combination of a tracked their preferred habitats from the densely sampled fossil record of Miocene Great Plains to the Gulf Coast (Webb et al. equids and detailed sedimentological infor- 1995). Within the Great Plains region, distri- mation available for the Great Plains allowed bution patterns show invasion of species from detailed quantitative projections of individual the southwest and an overall southward species’ geographic ranges not attainable migration of taxa from the Great Plains through traditional historical biogeographic toward the Gulf Coast. methods. 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