Introduction

Borophagines were a diverse and successful subfamily of canids that thrived throughout North America for nearly 30 million years. The group lived across the continent, and their fossils have been recovered from as far north as Saskatchewan, south into Mexico and Honduras, the Pacific Coast, and more recently along the Atlantic Coast (Wang et al., 1999; Eshelman and Whitmore, 2008; Wang and Tedford, 2008; Tseng and Geisler, 2016) (Table 1; Fig. 1). The majority of fossil localities where Borophagus is represented indicate environments dominated by relatively open habitats (grassland, savannah, and steppe), although some sites do indicate more extensive vegetation along streams and marshes, or more forested areas on their edges (Cook, 1922; Matthew, 1924, 1930; Matthew and Stirton, 1930; Meade, 1945; Dalquest, 1969; Bjork, 1970; Hulbert et al., 2009). Other vertebrates commonly found with Borophagus include equine and hipparionine horses (including Hipparion, Dinohippus, and Equus) (Cook, 1922; Matthew, 1924, 1930; Matthew and Stirton, 1930; Meade, 1945; Miller and Carranza-Castañeda, 1998; Hulbert et al., 2009), hornless rhinoceros (Aphelops and Teleoceras) (Matthew, 1924, 1930; Matthew and Stirton, 1930; Hulbert et al., 2009), camels (including Megatylopus, Hemiauchenia, and Camelops) (Cook, 1922; Matthew, 1924, 1930; Matthew and Stirton, 1930; Meade, 1945; Miller and Carranza-Castañeda, 1998; Hulbert et al., 2009), and mastodons (Matthew, 1930; Matthew and Stirton, 1930; Meade, 1945; Hulbert et al., 2009), which have been interpreted as suggesting grass-dominated habitats (Cook, 1922; Matthew, 1924, 1930; Matthew and Stirton, 1930; Meade, 1945; Hulbert et al., 2009).

Appendicular bones are important to understanding the ecology of carnivorans because their predatory behavior has driven the morphological evolution of their limbs (Van Valkenburgh, 1987; Samuels et al., 2013; Martín-Serra et al., 2016). In general, the anatomy of the forelimbs is very telling of the type of predatory behavior, whereas hind legs give a better indication of speed (Van Valkenburgh, 1987; Andersson and Werdelin, 2003; Andersson, 2005; Meachen-Samuels and Van Valkenburgh, 2009; Figueirido and Janis, 2011; Fabre et al., 2013; Samuels et al., 2013; Janis and Figueirido, 2014; Figueirido et al., 2015; Martín-Serra et al., 2016). Postcranial material of Borophagus has been recovered rarely, making their predatory behavior and locomotion controversial, because their appendicular skeleton is extremely different from modern members of Caninae (Dalquest, 1969; Munthe, 1989; Wang et al., 1999; Figueirido et al., 2015; Martín-Serra et al., 2016). Borophagus has limb proportions with longer proximal elements and shorter distal elements, leading to the inference that these dogs were not strongly running-adapted (Matthew, 1930; Dalquest, 1969; Munthe, 1989). Munthe (1989) hypothesized that the short and robust limbs of Borophagus would have been better adapted for closed habitats where open environments never formed, but with a lack of ecological data at the time, these hypotheses were not able to be assessed. Based on the skeletal and muscular morphology of Borophagus, it was interpreted as flexible and opportunistic in hunting strategies and habitats (Munthe, 1989). Figueirido et al. (2015) examined the elbow morphology of a wide range of fossil canids, and inferred secondarily derived ambush hunting predatory behavior in Borophagus. The habits of Borophagus in the late Neogene were noted to have contrasted with other canids at the time, which show a general trend toward greater cursorial specialization and pursuit-hunting habits, and further suggests a diversity of (open and closed) habitats were present in North America at the time (Figueirido et al., 2015).

Table 1.

Previously reported occurrences of Borophagus in North America. Data derived from the MIOMAP/FAUNMAP databases (Carrasco et al., 2007; Graham and Lundelius, 2010), NOW database (The NOW Community, 2019), and recent publications (Wang et al., 1999; Tseng and Geisler, 2016; Wang et al., 2018). AZ = Arizona; CA = California; CO = Colorado; FL = Florida; ID = Idaho; IN = Indiana; KS = Kansas; NC = North Carolina; NE = Nebraska; NM = New Mexico; NV = Nevada; OK = Oklahoma; OR = Oregon; SC = South Carolina; TN = Tennessee; TX = Texas; WA = Washington.

Continued.

Figure 1.

Distribution map of localities for Borophagus specimens. Data sources can be found in Table 1.

Given the site's age, an Early Pliocene locality located in northeastern Tennessee, the conspicuous absence of Borophagus from the Gray Fossil Site (GFS) was previously noted by multiple researchers (Wang and Tedford, 2008; Tseng and Geisler, 2016). A recently discovered canid humerus (Fig. 2) from GFS is described here as Borophagus. This new occurrence in the heavily forested Appalachian region can provide new insights on its distribution and ecology of the genus.

Geologic setting

The Gray Fossil Site in Washington County, Tennessee, is an Early Pliocene (late Hemphillian or early Blancan) fossil locality, which dates to ca. 4.9–4.5 Ma (Samuels et al., 2018). The site is located in the Appalachian forests of northeastern Tennessee, making it the only pre-Pleistocene vertebrate fossil locality in the Appalachian region of the eastern United States. Studies suggest that the site was formed when an ancient sinkhole collapsed, became a small lake, and then filled with sediment over several thousand years (Wallace and Wang, 2004; Shunk et al., 2006, 2009). This unique paleontological site records a diverse array of taxa, including a wide variety of flora, invertebrates, fish, amphibians, reptiles, birds, and small and large mammals (Parmalee et al., 2002; Wallace and Wang, 2004; DeSantis and Wallace, 2008; Boardman and Schubert, 2011; Zobaa et al., 2011; Mead et al., 2012; Ochoa et al., 2012, 2016; Worobiec et al., 2013; Bourque and Schubert, 2015; Jasinski and Moscato, 2017; Jasinski, 2018; Short et al., 2019; Siegert and Hermsen, 2020; Quirk and Hermsen, 2021). Flora and fauna at the site have been interpreted to indicate a relatively closed forested ecosystem (Ochoa et al., 2016; Samuels et al., 2018; Quirk and Hermsen, 2021). To date, the only carnivorans described from the site are an ailurid, Pristinailurus bristoli Wallace and Wang, 2004, a meline badger, Arctomeles dimolodontus Wallace and Wang, 2004, and the earliest record of a wolverine, Gulo sudorus Samuels, Bredehoeft, and Wallace, 2018. Wallace and Wang (2004) also noted the presence of Plionarctos sp., cf. Machairodus sp., and “Canidae” in their faunal list.

Figure 2.

Borophagus sp. (ETMNH 10545) from the Gray Fossil Site, Tennessee. (1) Anterior, (2) posterior, (3) medial, (4) lateral views. Scale bar = 1 cm.

Materials and methods

The GFS fossil canid specimen was qualitatively and quantitatively compared to a broad sample of extant and fossil canids (from Samuels et al., 2013), as well as published descriptions from a variety of sources (Dalquest, 1969; Munthe, 1989; Wang et al., 1999). Measurements followed Samuels et al. (2013) and were taken to the nearest 0.01 mm using digital calipers, these include: total length of the humerus (HuL), anterioposterior diameter (HuAPD), mediolateral diameter (HuMLD), length of pectoral crest (HuPCL), epicondylar breadth of the distal humerus (HuEB), and breadth of the distal articular surface (HuHTL). These six measurements were used to compare the humeral proportions among species, and also to calculate three functional indices (Table 2; Fig. 3) used in a variety of studies (Samuels et al., 2013). The overall sample includes 20 extant canid species, from 13 genera, and 20 fossil species, with members of all three canid subfamilies represented (complete data are provided in Table 3). Raw measurements and indices were used in linear regressions to make inferences about the limb proportions, locomotor habits, and body size of the canid from GFS using IBM SPSS Statistics 24. Body mass of the GFS specimen was estimated using published regression equations from Anyonge (1993) and Figuerido et al. (2011).

Table 2.

Morphological indices used in the analyses, their definitions, and their inferred functional significance.

Repositories and institutional abbreviations.—The figured specimen examined in this study is deposited in the East Tennessee State University Museum of Natural History (ETMNH), Tennessee, USA. Additional specimens measured in this study are reposited in the American Museum of Natural History (F:AM), National Museum of Natural History (USNM), Midwestern University (MU), and University of California Museum of Paleontology (UCMP).

Systematic paleontology

Figure 3.

Linear regression comparisons of humeral proportions among canid species. See Table 3 for species list. (1) Log/log plot of humerus length against anteroposterior diameter, (2) log/log plot of humerus length against mediolateral diameter, (3) log/log plot of humerus length against deltopectoral crest length, (4) log/log plot of humerus length against epicondylar breadth, (5) log/log plot of humerus length against trochanter length, (6) log/log plot of epicondylar breadth against trochanter length. Extinct taxa are denoted by † symbol.

Table 3.

Humerus measurements (in mm) of Borophagus sp. from the Gray Fossil Site, and species mean values for a comparative sample of extant and fossil canids. Measurements for other canids derived from Samuels et al. (2013): Alopex lagopus Linnaeus, 1758; Atelocynus microtis (Sclater, 1882); Canis adustus Sundevall, 1846; Canis latrans Say, 1823a; Canis mesomelas Hilzheimer, 1906; Cerdocyon thous (Linnaeus, 1766); Cuon alpinus (Pallas, 1811); Lycalopex gymnocerus Fischer de Waldheim, 1814; Otocyon megalotis (Desmarest, 1822); Urocyon cinereoargenteus (Schreber, 1775); Urocyon littoralis (Baird, 1857); Vulpes macrotis Merriam, 1888; Vulpes vulpes Linnaeus, 1758; Vulpes zerda (Zimmerman, 1780); Aelurdon asthenostylus (Henshaw, 1942); Aelurdon ferox Leidy, 1858; Aelurdon taxoides (Hatcher, 1893); Archaeocyon stirtoni (Webb, 1969b); Archaeocyon leptodus Schlaikjer, 1935; Cynarctus crucidens Barbour and Cook, 1914; Desmocyon thomsoni (Matthew, 1907); Epicyon saevus (Leidy, 1858); Tomarctus robustus (Green, 1948); Mesocyon coryphaeus (Cope, 1884). Extinct species are denoted by a † symbol.

Results

Age and body size.—A study by von Pfeil et al. (2009) examined the epiphyseal plates in modern canids and found that most domestic dogs reach 90% of their adult size by 10 months, with the majority of growth plates fusing between 4–12 months. The proximal humeral epiphysis fully fuses between 10–12 months of age, while the distal humeral epiphysis fuses earlier, between 5–8 months (von Pfeil et al., 2009). The distal epiphysis of the humerus from the GFS specimen is fully fused, but the proximal epiphysis is partially fused, suggesting the GFS specimen is most likely between the ages of 8–12 months. A body mass estimate was calculated using published equations; the formula provided by Anyonge (1993) yielded a body mass estimate of 74.13kg, while that of Figuerido et al. (2011) produced a body mass estimate of 52.48kg.

Morphometric comparison.—The length of the GFS humerus (ETMNH 10545) is greater than most other canids studied, with the exception of the gray wolf (Canis lupus Linnaeus, 1758), African hunting dog (Lycaon pictus Griffith, Smith, and Pidgeon, 1827), dire wolf (Canis dirus Leidy, 1858), and Armbruster's wolf (Canis armbrusteri) (Table 3). The GFS canid has a very robust shaft (Table 3) and only one other canid studied has a larger diaphyseal diameter; C. dirus. Three other species, C. lupus, C. armbrusteri Gidley, 1913, and the maned wolf (Chrysocyon brachyurus [Illiger, 1815]), have greater mediolateral diameter. The deltopectoral crest length of ETMNH 10545 is relatively large (Table 3), only C. lupus, C. dirus, and C. brachyurus have greater lengths, and each of those taxa has a much longer overall humerus length, meaning the GFS canid has a proportionately longer pectoral crest and thus shoulder moment index (SMI) (Fig. 3). The epicondylar breadth of ETMNH 10545 is the second largest of the canids studied, only behind the much larger C. dirus, but the relative size of the epicondyles (HEB) is much greater than C. dirus and all other canids studied, with exception of the early hesperocyonine Paraenhydrocyon josephi (Cope, 1881) (Table 3; Fig. 3). The distal articular surface, including the capitulum and trochlea, is very broad in specimens of Borophagus, greater than all other studied taxa, with exception of the borophagine Epicyon haydeni Leidy, 1858, which is also much larger and relatively broader (compared to humerus length) than in any other canid (Table 3). The shoulder moment index is >0.5 in ETMNH 10545 (Table 3) and in the early canids Hesperocyon gregarius Wortman and Matthew, 1899, Paraenhydrocyon josephi, and Phlaocyon leucosteus Matthew, 1899, and the extant Nyctereutes procyonoides (Gray, 1834) and Speothos venaticus (Lund, 1842). The humeral robustness (HRI) of C. dirus, H. gregarius, and P. josephi is greater than the GFS specimen (Table 3).

Discussion

Recovered postcranial elements of Borophagus are rare, with only 16 specimens having been reported from the fossil record (Dalquest, 1969; Munthe, 1989; Wang et al., 1999). The addition of the GFS humerus aides in understanding the ecology of the genus, both in terms of locomotion and habitat preference. While the humerus is attributable to the genus Borophagus, there was not enough evidence to assign a species; however, based on the age and morphology of the humerus, the most likely contender is B. diversidens.

The two body mass estimates for Borophagus produced here, 52.48 kg and 74.13 kg, are larger than the average mass of the modern gray wolf (Canis lupus). Figueirido et al. (2015) provided estimated body mass for several species of Borophagus based on the humerus, with estimated masses of B. parvus = 34.5 kg, B. pugnator = 58.5 kg, and B. secundus = 33.1 kg and 39.1 kg. These estimates are fairly similar, indicating relatively large body mass in Borophagus and supporting inference of predatory specialization for larger taxa (Carbone et al., 1999, 2007). Cursorial carnivorans have generally gracile limbs characterized by low HRI and have smaller humeral epicondyles, while semifossorial and semiaquatic carnivorans have enlarged humeral epicondyles to allow for larger area for forearm flexor, pronator, and supinator muscles (Samuels et al., 2013). Humeri in non-cursorial canid taxa are relatively robust, likely as a consequence of ambush predatory behavior, which demands short bursts of speed and extra strength to take down prey (Van Valkenburgh, 1985; Munthe, 1989; Anyonge, 1996; Figueirido et al., 2015; Martín-Serra et al., 2016). Extant ambush predators have a humeral head that is posteriorly oriented and an anteroposteriorly convex shaft; attributes that suggest the humerus is flexed when taking down prey (Martín-Serra et al., 2016). Additionally, ambush predators have a large medial epicondyle where the flexor muscles would attach and increase the ability to grasp prey (Martín-Serra et al., 2016). A shallow trochlea allows supination of the forearm (Andersson, 2005; Figueirido and Janis, 2011; Janis and Figueirido, 2014; Figueirido et al., 2015; Martín-Serra et al., 2016), but also indicates long-distance running is not a specialty; instead, animals possessing such features have the ability to perform a variety of tasks (Munthe, 1989; Fabre et al., 2013; Figueirido et al., 2015; Martín-Serra et al., 2016). The presence of a shallow trochlea with a circular-shaped diaphysis cross section allows movement of the forearm to occur outside the parasagittal plane (Figueirido and Janis, 2011; Janis and Figueirido, 2014; Figueirido et al., 2015; Martín-Serra et al., 2016).

The GFS specimen possesses all features of those seen in ambush predator humeri, and given the presence of a heavily forested habitat, for which rapid locomotion was not well suited, Borophagus most likely would have been an ambush predator. Additionally, the presence of Borophagus in Honduras (and now eastern Tennessee), which are parts of North America that never transitioned to open grassland or steppe environments, could suggest Borophagus was adapted to live in both open- and closed-habitat environments (Munthe, 1989).

The shoulder moment index (SMI) of ETMNH 10545 is similar to Hesperocyon gregarious, Paraenhydrocyon josephi, and Phlaocyon leucosteus, indicating a high mechanical advantage across the shoulder joint (Fig. 3). Paraenhydrocyon josephi, an early member of the hesperocyonine subfamily, was adapted for a semi-arboreal lifestyle, while H. gregarious evolved in a forested environment. The humeral robustness indices (HRIs) of C. dirus, H. gregarious, and P. josephi are similar to the GFS specimen (Fig. 3). The relative size of the humeral epicondyles (HEB) in ETMNH 10545 is much greater than all other canids studied, other than P. josephi, and quite distinct from the relatively narrow epicondyles of cursorially adapted pursuit predators (Fig. 3). The large medial epicondyle would have provided for large areas of origin for the wrist and digital flexors, which would have facilitated grasping movements that are typical of ambush hunting predators. Due to the somewhat similar dimensions with the four taxa listed above, it can be concluded the GFS Borophagus was not well adapted for running long distances and most likely was not a pursuit predator. Borophagus may have spent some of its time digging, possibly for refuge from larger competitors (given its size, it needed to feed on prey 50% of its size) (Carbone et al., 1999, 2007).

Borophagus has been found to inhabit grasslands, transitional, coastal, and now forested habitats. Skeletal and muscular morphology indicate the genus was not adapted for a cursorial lifestyle, which would have been problematic because of their highly cursorial prey. It is thought Borophagus may have been a social animal, and in packs could have hunted larger prey (Wang et al., 2018). This method may have suited Borophagus in open environments, but specimens found in forested environments, where their skeletal morphology may have been more functionally adapted, may not have needed these pack hunting skills because the forests would have provided sufficient cover for an ambush attack.

Conclusions

The GFS humerus identified as belonging to Borophagus sp. is the first occurrence of the genus in Tennessee and in a heavily forested ecosystem. Weighing between 52–74 kg, the GFS Borophagus is interpreted as adapted to an ambush predatory lifestyle in a closed forested habitat, distinct from the cursorial locomotion other canids living in open habitats. Borophagus would have been one of the largest predators in the GFS forest, alongside saber-toothed cats, and with an abundance of tapirs (Tapirus polkensis Olsen, 1960) and other large herbivores at the site, there certainly would have been enough food resources to support both apex predators.